Reid - Biological Emergences Evolution by Natural Experiment (2007) PDF

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Biological Emergences
philosophy/biology/evolution The Vienna Series in Theoretical Biology
Evolution by Natural Experiment
Robert G. B. Reid
Natural selection is commonly interpreted as the fundamental mechanism of evolution.

Questions about how selection theory can claim to be the all-sufficient explanation of evolu-
tion often go unanswered by todays neo-Darwinists, perhaps for fear that any criticism of
the evolutionary paradigm will encourage creationists and proponents of intelligent design.
In Biological Emergences, Robert Reid argues that natural selection is not the cause of
evolution. He writes that the causes of variations, which he refers to as natural experiments,
are independent of natural selection; indeed, he suggests, natural selection may get in the
way of evolution. Reid proposes an alternative theory to explain how emergent novelties Evolution by Natural Experiment
are generated and under what conditions they can overcome the resistance of natural
selection. He suggests that what causes innovative variation causes evolution, and that these
phenomena are environmental as well as organismal.
After an extended critique of selectionism, Reid constructs an emergence theory of
evolution, first examining the evidence in three causal arenas of emergent evolution: sym- Robert G. B. Reid
biosis/association, evolutionary physiology/behavior, and developmental evolution. Based
Reid
on this evidence of causation, he proposes some working hypotheses, examining mech-
anisms and processes common to all three arenas, and arrives at a theoretical framework
that accounts for generative mechanisms and emergent qualities. Without selectionism, Reid
argues, evolutionary innovation can more easily be integrated into a general thesis. Finally,
Reid proposes a biological synthesis of rapid emergent evolutionary phases and the pro-
longed, dynamically stable, non-evolutionary phases imposed by natural selection.
Robert G. B. Reid is Emeritus Professor of Biology at the University of Victoria, British

Columbia. He is the author of Evolutionary Theory: The Unfinished Synthesis.
Vienna Series in Theoretical Biology
This book is a grand synthesis of historical evolutionism and modern biology from an author
with wide experience in teaching, research, reflection, and argument on the subject. Its
stance is inclusive, its style candid and engaging. Biological Emergences is entirely success-
ful in outlining an alternative to natural selectionism, a viable theory about the origin of things
rather than their ultimate survival or extinction. This book maynay, shouldbe profitably
read by anyone interested in evolution and its meaning within human understanding.
Gareth Nelson, School of Botany, University of Melbourne
The MIT Press

Massachusetts Institute of Technology
Cambridge, Massachusetts 02142
http://mitpress.mit.edu
978-0-262-18257-7
0-262-18257-2
The Vienna Series in Theoretical Biology
Gerd B. Mller, Gnter P. Wagner, and Werner Callebaut, editors
The Evolution of Cognition, edited by Cecilia Heyes and Ludwig Huber, 2000
Origination of Organismal Form: Beyond the Gene in Developmental and Evolutionary Biology, edited
by Gerd B. Mller and Stuart A. Newman, 2003
Environment, Development, and Evolution: Toward a Synthesis, edited by Brian K. Hall, Roy D.
Pearson, and Gerd B. Mller, 2004
Evolution of Communication Systems: A Comparative Approach, edited by D. Kimbrough Oller and

Ulrike Griebel, 2004
Modularity: Understanding the Development and Evolution of Natural Complex Systems, edited by
Werner Callebaut and Diego Rasskin-Gutman, 2004
Compositional Evolution: The Impact of Sex, Symbiosis, and Modularity on the Gradualist Framework
of Evolution, Richard A. Watson, 2005
Biological Emergences: Evolution by Natural Experiment, Robert G. B. Reid, 2007

Evolution by Natural Experiment
Robert G. B. Reid
A Bradford Book
The MIT Press
Cambridge, Massachusetts
London, England
2007 Massachusetts Institute of Technology
All rights reserved. No part of this book may be reproduced in any form by any electronic or
mechanical means (including photocopying, recording, or information storage and retrieval)
without permission in writing from the publisher.
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Set in Stone by The MIT Press. Printed and bound in the United States of America.
Library of Congress Cataloging-in-Publication Data
Reid, Robert G. B., 1939

Biological emergences : evolution by natural experiment / Robert G.B. Reid.
p. cm. (Vienna series in theoretical biology)
Includes bibliographical references (p. ).
ISBN-13: 978-0-262-18257-7 (alk. paper)
ISBN-10: 0-262-18257-2 (hardcover : alk. paper)
1. Evolution (Biology) 2. Variation (Biology) I. Title.
QH366.2.R45 2007
576.8dc22
2006049132
10 9 8 7 6 5 4 3 2 1
To Clio.
This is the age of the evolution of Evolution. All thoughts that the Evolutionist works with, all
theories and generalizations, have themselves evolved and are now being evolved. Even were his
theory perfected, its first lesson would be that it was itself but a phase of the Evolution of other
opinion, no more fixed than a species, no more final than the theory which it displaced.
Henry Drummond, 1883
Contents
Series Foreword xi
Preface xiii
Introduction: The Re-invention of Natural Selection 1
1 Paradigm Drift 27
2 Prologue to Emergence 67
3 Evolution by Association 95
4 The Physiological Arena 137
5 Development and Evolution 179
6 Epigenetic Mechanisms 223
7 Orthogenesis 267
8 The Re-invention of Emergence 289
9 From the Particular to the General 329
10 An Emergence Theory 363
11 A Biological Synthesis 401
Notes 437
Bibliography 465
Index 505
Series Foreword
Biology is becoming the leading science in this century. As in all other sciences,
progress in biology depends on interactions between empirical research, theory
building, and modeling. But whereas the techniques and methods of descriptive and
experimental biology have evolved dramatically in recent years, generating a flood of
highly detailed empirical data, the integration of these results into useful theoretical
frameworks has lagged behind. Driven largely by pragmatic and technical considera-
tions, research in biology continues to be less guided by theory than seems indicated.
By promoting the formulation and discussion of new theoretical concepts in the bio-
sciences, this series intends to help fill the gaps in our understanding of some of the
major open questions of biology, such as the origin and organization of organismal
form, the relationship between development and evolution, and the biological bases
of cognition and mind.
Theoretical biology has important roots in the experimental biology movement of
early-twentieth-century Vienna. Paul Weiss and Ludwig von Bertalanffy were among
the first to use the term theoretical biology in a modern scientific context. In their
understanding the subject was not limited to mathematical formalization, as is often
the case today, but extended to the conceptual problems and foundations of biology.
It is this commitment to a comprehensive, cross-disciplinary integration of theoretical
concepts that the present series intends to emphasize. Today theoretical biology has
genetic, developmental, and evolutionary components, the central connective themes
in modern biology, but also includes relevant aspects of computational biology,
semiotics, and cognition research, and extends to the naturalistic philosophy of
sciences.
The Vienna Series grew out of theory-oriented workshops organized by the
Konrad Lorenz Institute for Evolution and Cognition Research (KLI), an international
center for advanced study closely associated with the University of Vienna. The KLI
fosters research projects, workshops, archives, book projects, and the journal
Biological Theory, all devoted to aspects of theoretical biology, with an emphasis on
xii Series Foreword
integrating the developmental, evolutionary, and cognitive sciences. The series editors
welcome suggestions for book projects in these fields.
Gerd B. Mller, University of Vienna and KLI

Gnter P. Wagner, Yale University and KLI
Werner Callebaut, Hasselt University and KLI
Preface
Charles Darwin described The Origin of Species as one long argument for evolution
by natural selection. Subsequently Ernst Mayr applied the expression to the
continuing debate over Darwins ideas. My explanation of why the debate lingers is
that although Darwin was right about the reality of evolution, his causal theory was
fundamentally wrong, and its errors have been compounded by neo-Darwinism. In
1985 my book Evolutionary Theory: The Unfinished Synthesis was published. In it I
discussed Darwinian problems that have never been solved, and the difficulties
suffered historically by holistic approaches to evolutionary theory. The most
important of these holistic treatments was emergent evolution, which enjoyed a
brief moment of popularity about 80 years ago before being eclipsed when natural
selection was mathematically formalized by theoretical population geneticists. I saw
that the concept of biological emergence could provide a matrix for a reconstructed
evolutionary theory that might displace selectionism. At that time, I naively thought
that there was a momentum in favor of such a revision, and that there were enough
open-minded, structuralistic evolutionists to displace the selectionist paradigm within
a decade or so. Faint hope!
Instead, the conventional Modern Synthesis produced extremer forms of selec-
tionism. Although some theoreticians were dealing effectively with parts of the
problem, I decided I should try again, from a more general biological perspective. This
book is the result.
The main thrust of the book is an exploration of evolutionary innovation, after a
critique of selectionism as a mechanistic explanation of evolution. Yet it is impossible
to ignore the fact that the major periods of biological history were dominated by
dynamic equilibria where selection theory does apply. But emergentism and selection-
ism cannot be synthesized within an evolutionary theory. A biological synthesis is
necessary to contain the history of life. I hope that selectionists who feel that I have
defiled their discipline might find some comfort in knowing that their calculations
and predictions are relevant for most of the 3.5 billion years that living organisms
have inhabited the Earth, and that they forgive me for arguing that those calculations
and predictions have little to do with evolution.
xiv Preface
Evolution is about change, especially complexifying change, not stasis. There are
ways in which novel organisms can emerge with properties that are not only self-
sufficient but more than enough to ensure their status as the founders of kingdoms,
phyla, or orders. And they have enough generative potential to allow them to diversify
into a multiplicity of new families, genera, and species. Some of these innovations are
all-or-none saltations. Some of them emerge at thresholds in lines of gradual and
continuous evolutionary change. Some of them are largely autonomous, coming from
within the organism; some are largely imposed by the environment. Their adaptive-
ness comes with their generation, and their adaptability may guarantee success
regardless of circumstances. Thus, the filtering, sorting, or eliminating functions of
natural selection are theoretically redundant.
Therefore, evolutionary theory should focus on the natural, experimental
generation of evolutionary changes, and should ask how they lead to greater
complexity of living organisms. Such progressive innovations are often sudden, and
have new properties arising from new internal and external relationships. They are
emergent. In this book I place such evolutionary changes in causal arenas that I liken
to a three-ring circus. For the sake of bringing order to many causes, I deal with the
rings one at a time, while noting that the performances in each ring interact with each
other in crucial ways. One ring contains symbioses and other kinds of biological asso-
ciation. In another, physiology and behavior perform. The third ring contains of
developmental or epigenetic evolution.
After exploring the generative causes of evolution, I devote several chapters to sub-
theories that might arise from them, and consider how they might be integrated into
a thesis of emergent evolution. In the last chapter I propose a biological synthesis.
In the bibliographical introduction to the reference section of this book I acknowl-
edge authors who inspired me to return to the fray. Here I acknowledge family, friends,
and colleagues who helped and encouraged me. First and foremost is my daughter
Clio, who was my front-line editor during the development of this work. Once I had
produced the first draft, my personal readers were, in order of recruitment, Clio (now
studying parrot behavior as a graduate student at Victoria University of Wellington,
New Zealand); the zoologist Louise Russert-Kraemer of the University of Arkansas; the
social psychologist Bill Livant, formerly of the University of Regina; and the
biochemist Rodney Roche of the University of Calgary. Particular thanks go to Rodney,
who read two subsequent versions of the manuscript and provided much help with
references. I am also grateful to the molecular biologist Kevin Little, now at the
University of Auckland, who was very helpful with the epigenetics chapter. The micro-
biologist Lee Haines was an enthusiastic informant on insect endosymbionts. The
historian of medical biology Judith Friedmann introduced me to the subject of antic-
ipation diseases, as well as making helpful general comments along the way. Kathy
Wynne-Edwards gave me the full story of the Siberian hamster, an iconic illustration
Preface xv
of how physiological evolution can work. Elisabeth Vrba had a catalytic influence on
the progress of this works publication, as well as providing me with many of her
important publications.
Some of my students were directly involved in my study of evolutionary theory. At
the risk of alienating the many, I would mention a few of the more recent ones:
Camilla Berry, Carol Hartwig, Ben Geselbracht, Kevin Peterson, John Simaika, and Will
Duguid. My regular evolutionary sparring partners are Richard Ring, Bill Livant, and
Tom Reimchen, and my cheering section includes Dawna Brand, Eugene Balon, Roy
Pearson, Rene Hetherington, and Gizelle Rhyon-Berry. Members of the Department
of Biology at the University of Victoria, including Louise Page, Tom Reimchen, Richard
Ring, George Mackie, John Taylor, Gerry Allen, and Nancy Sherwood, willingly
provided reference material along with librarian Kathleen Matthews. Once the
manuscript was ready to submit for publication, Gerd Mller and Werner Callebaut,
editors of the Vienna Series in Theoretical Biology, responded very enthusiastically.
They continued to give me solid encouragement and support through the editing and
revision stages. I am also grateful for the hospitality of the Konrad Lorenz Institute on
two occasions during the development of this work.
Introduction
The Re-invention of Natural Selection
I regard it as unfortunate that the theory of natural selection was first developed as an
explanation for evolutionary change. It is much more important as an explanation for the
maintenance of adaptation.
George Williams, 19661
Natural selection cannot explain the origin of new variants and adaptations, only their spread.
John Endler, 19862
We could, if we wished, simply replace the term natural selection with dynamic stabilization. . . .
Brian Goodwin, 19943
Nobody is going to re-invent natural selection. . . .

Nigel Hawkes, 19974
Ever since Charles Darwin published The Origin of Species, it has been widely believed
that natural selection is the primary cause of evolution. However, while George
Williams and John Endler take the trouble to distinguish between the causes of
variation and what natural selection does with them; the latter is what matters to
them. In contrast, Brian Goodwin does not regard natural selection as a major evolu-
tionary force, but as a process that results in stable organisms, populations, and
ecosystems. He would prefer to understand how evolutionary novelties are generated,
a question that frustrated Darwin for all of his career.
During the twentieth century, Darwins followers eventually learned how
chromosomal recombination and gene mutation could provide variation as fuel for
natural selection. They also re-invented Darwinian evolutionary theory as neo-
Darwinism by formalizing natural selection mathematically. Then they redefined it as
differential survival and reproduction, which entrenched it as the universal cause of
evolution. Nigel Hawkess remark that natural selection cannot be re-invented demon-
strates its continued perception as an incorruptible principle. But is it even a minor
cause of evolution?
2 Introduction
Natural selection supposedly builds order from purely random accidents of nature
by preserving the fit and discarding the unfit. On the face of it, that makes more than
enough sense to justify its importance. Additionally, it avoids any suggestion that a
supernatural creative hand has ever been at work. But it need not be the only
mechanistic option. And the current concept of natural selection, which already has
a history of re-invention, is not immune to further change. Indeed, if its present inter-
pretation as the fundamental mechanism of evolution were successfully challenged,
some of the controversies now swirling around the modern paradigm might be
resolved.
A Paradigm in Crisis?
Just what is the evolutionary paradigm that might be in crisis? It is sometimes called
the Modern Synthesis. Fundamentally it comes down to a body of knowledge, inter-
pretation, supposition, and extrapolation, integrated with the belief that natural
selection is the all-sufficient cause of evolutionif it is assumed that variation is
caused by gene mutations. The paradigm has built a strong relationship between
ecology and evolution, and has stimulated a huge amount of research into population
biology. It has also been the perennial survivor of crises that have ebbed and flowed
in the tide of evolutionary ideas. Yet signs of discord are visible in the strong polariza-
tion of those who see the whole organism as a necessary component of evolution and
those who want to reduce all of biology to the genes. Since neo-Darwinists are also
hypersensitive to creationism, they treat any criticism of the current paradigm as a
breach of the scientific worldview that will admit the fundamentalist hordes.
Consequently, questions about how selection theory can claim to be the all-sufficient
explanation of evolution go unanswered or ignored. Could most gene mutations be
neutral, essentially invisible to natural selection, their distribution simply adrift? Did
evolution follow a pattern of punctuated equilibrium, with sudden changes separated
by long periods of stasis? Were all evolutionary innovations gene-determined? Are
they all adaptive? Is complexity built by the accumulation of minor, selectively advan-
tageous mutations? Are variations completely random, or can they be directed in some
way? Is the generation of novelty not more important than its subsequent selection?
Long before Darwin, hunters, farmers, and naturalists were familiar with the process
that he came to call natural selection. And they had not always associated it with
evolution. It is recognized in the Bible, a Special Creation text. Lamarck had thought
that evolution resulted from a universal progressive force of nature, not from natural
selection. Organisms responded to adaptational needs demanded by their environ-
ments. The concept of adaptation led Lamarcks rival, Georges Cuvier, to argue the
opposite. If existing organisms were already perfectly adapted, change would be
detrimental, and evolution impossible. Nevertheless, Cuvier knew that biogeography
The Re-invention of Natural Selection 3
and the fossil record had been radically altered by natural catastrophes. These Darwin
treated as minor aberrations during the long history of Earth. He wanted biological
and geographical change to be gradual, so that natural selection would have time to
make appropriate improvements. The process of re-inventing the events themselves to
fit the putative mechanism of change was now under way.
Gradualism had already been brought to the fore when geologists realized that what
was first interpreted as the effects of the sudden Biblical flood was instead the result of
prolonged glaciation. Therefore, Darwin readily fell in with Charles Lyells belief that
geological change had been uniformly slow. Now, more than a century later, catas-
trophism has been resurrected by confirmation of the K-T (Cretaceous-Tertiary) bolide
impact that ended the Cretaceous and the dinosaurs. Such disasters are also linked to
such putative events as the Cambrian Big Bang of Biology, when all of the major
animal phyla seem to have appeared almost simultaneously.5 The luck of the draw has
returned to evolutionary theory. Being in the right place at the right time during a
cataclysm might have been the most important condition of survival and subsequent
evolution.
Beyond the fringe of Darwinism, there are heretics who believe the neo-Lamarckist
tenet that the environment directly shapes the organism in a way that can be passed
on from one generation to the next. They argue that changes imposed by the
environment, and by the behavior of the organism, are causally prior to natural
selection. Nor is neo-Lamarckism the only alternative. Some evolutionary biologists,
for example, think that the establishment of unique symbioses between different
organisms constituted major evolutionary novelties. Developmental evolutionists are
reviewing the concept that evolution was not gradual but saltatory (i.e., advancing in
leaps to greater complexity). However, while they emphasize the generation of evolu-
tionary novelty, they accommodate natural selection as the complementary and
essential causal mechanism.
Notes on isms
Before proceeding further, I want to explain how I arbitrarily, but I hope consistently,
use the names that refer to evolutionary movements and their originators.
Darwinian and Lamarckian refer to any idea or interpretation that Darwin and
Lamarck originated or strongly adhered to. Darwinism is the paradigm that rose from
Darwinian concepts, and Lamarckism is the movement that followed Lamarck. They
therefore include ideas that Darwin and Lamarck may not have thought of nor
emphasized, but which were inspired by them and consistent with their thinking.
Lamarck published La philosophie zoologique in 1809, and Lamarckism lasted for about
80 years until neo-Lamarckism developed. Darwinism occupied the time frame
between the publication of The Origin of Species (1859) and the development of neo-
4 Introduction
Darwinism. The latter came in two waves. The first was led by August Weismann, who
was out to purify evolutionary theory of Darwinian vacillation. The second wave,
which arose in theoretical population genetics in the 1920s, quantified and redefined
the basic tenets of Darwinism. Selectionism is the belief that natural selection is the
primary cause of evolution. Its influence permeates the Modern Synthesis, which was
originally intended to bring together all aspects of biology that bear upon evolution
by natural selection. Niles Eldredge (1995) uses the expression ultra-Darwinian to
signify an extremist position that makes natural selection an active causal evolution-
ary force. For grammatical consistency, I prefer ultra-Darwinist, which was used in
the same sense by Pierre-Paul Grass in 1973.6
The Need for a More Comprehensive Theory
I have already hinted that the selectionist paradigm is either insufficient to explain
evolution or simply dead wrong. Obviously, I want to find something better. Neo-
Darwinists themselves concede that while directional selection can cause adaptational
change, most natural selection is not innovative. Instead, it establishes equilibrium by
removing extreme forms and preserving the status quo. John Endler, the neo-
Darwinist quoted in one of this chapters epigraphs, is in good company when he says
that novelty has to appear before natural selection can operate on it. But he is silent
on how novelty comes into being, and how it affects the internal organization of the
organismquestions much closer to the fundamental process of evolution. He is not
being evasive; the issue is just irrelevant to the neo-Darwinist thesis.
Darwin knew that nature had to produce variations before natural selection could
act, so he eventually co-opted Lamarckian mechanisms to make his theory more com-
prehensive. The problem had been caught by other evolutionists almost as soon as The
Origin of Species was first published. Sir Charles Lyell saw it clearly in 1860, before he
even became an evolutionist:
If we take the three attributes of the deity of the Hindoo Triad, the Creator, Brahmah, the
preserver or sustainer, Vishnu, & the destroyer, Siva, Natural Selection will be a combination of
the two last but without the first, or the creative power, we cannot conceive the others having
any function.7
Consider also the titles of two books: St. George Jackson Mivarts On the Genesis of
Species (1872) and Edward Copes Origin of the Fittest (1887). Their play on Darwins
title emphasized the need for a complementary theory of how new biological
phenomena came into being. Soon, William Batesons Materials for the Study of
Variation Treated with Especial Regard to Discontinuity in the Origin of Species (1894) was
to distinguish between the emergent origin of novel variations and the action of
natural selection.
Figure I.1
The three-ring circus of evolutionary causation, under the big top of the environment.
The present work resumes the perennial quest for explanations of evolutionary
genesis and will demonstrate that the stock answerpoint mutations and recombina-
tions of the genes, acted upon by natural selectiondoes not suffice. There are many
circumstances under which novelties emerge, and I allocate them to arenas of evolu-
tionary causation that include association (symbiotic, cellular, sexual, and social),
functional biology (physiology and behavior), and development and epigenetics.
Think of them as three linked circus rings of evolutionary performance, under the big
top of the environment. Natural selection is the conservative ringmaster who ensures
that tried-and-true traditional acts come on time and again. It is the underlying
syndrome that imposes dynamic stabilityits hypostasis (a word that has the
additional and appropriate meaning of significant constancy).8
Selection as Hypostasis
The stasis that natural selection enforces is not unchanging inertia. Rather, it is a state
of adaptational and neutral flux that involves alterations in the numerical proportions
of particular alleles and types of organism, and even minor extinctions. It does not
produce major progressive changes in organismal complexity. Instead, it tends to lead
to adaptational specialization. Natural selection may not only thwart progress toward
greater complexity, it may result in what Darwin called retrogression, whereby
complex and adaptable organisms revert to simplified conditions of specialization.
This is common among parasites, but not unique to them. For example, our need for
ascorbic acidvitamin Cresults from the regression of a synthesis pathway that was
functional in our mammalian ancestors.
On the positive side, it may be argued that dynamic stability, at any level of organ-
ization, ensures that the foundations from which novelties emerge are solid enough
to support them on the rare occasions when they escape its hypostasis. A world devoid
of the agents of natural selection might be populated with kludgesgimcrack
organisms of the kind that might have been designed by Heath Robinson, Rube
6 Introduction
Goldberg, or Tim Burton. The enigmatic bizarre and dream-like Hallucigenia of the
Burgess Shale springs to mind.9 Even so, if physical and embryonic factors constrain
some of the extremest forms before they mature and reproduce, the benefits of natural
selection are redundant. Novelty that is first and foremost integrative (i.e., allows the
organism to operate better as a whole) has a quality that is resistant to the slings and
arrows of selective fortune.
Natural selection has to do with relative differences in survival and reproduction
and the numerical distribution of existent variations that have already evolved. In this
form it requires no serious re-invention. But selectionism goes on to infer that natural
selection creates complex novelty by saving adaptive features that can be further built
upon. Such qualities need no saving by metaphorical forces. Having the fundamental
property of persistence that characterizes life, they can look after themselves. As
Ludwig von Bertalanffy remarked in 1967, favored survival of better precursors of
life presupposes self-maintaining, complex, open systems which may compete;
therefore natural selection cannot account for the origin of those symptoms.10 These
qualities were in the nature of the organisms that first emerged from non-living
origins, and they are prior to any action of natural selection. Compared to them,
ecological competitiveness is a trivial consequence.
But to many neo-Darwinists the only real evolution is just that: adaptationthe
selection of random genetic changes that better fit the present environment.
Adaptation is appealingly simple, and many good little examples crop up all the time.
However, adaptation only reinforces the prevailing circumstances, and represents but
a fragment of the big picture of evolution. Too often, genetically fixed adaptation is
confused with adaptabilitythe self-modification of an individual organism that
allows responsiveness to internal and external change. The logical burden of selection-
ism is compounded by the universally popular metaphor of selection pressure, which
under some conditions of existence is supposed to force appropriate organismic
responses to pop out spontaneously. How can a metaphor, however heuristic, be a
biological cause? As a metaphor, it is at best is an inductive guide that must be used
with caution.
Even although metaphors cannot be causes, their persuasive powers have given
natural selection and selection pressure perennial dominance of evolutionary theory.
It is hard enough to sideline them, so as to get to generative causes, far less to convince
anyone that they are obstructive. Darwin went so far as to make this admission:
In the literal sense of the word, no doubt, natural selection is a false term. . . . It has been said
that I speak of natural selection as an active power or Deity. . . . Everyone knows what is meant
and is implied by such metaphorical expressions; and they are almost necessary for brevity. . . .
With a little familiarity such superficial objections will be forgotten.11
Alas, in every subsequent generation of evolutionists, familiarity has bred contempt as

well as forgetfulness for such superficial objections.
Are All Changes Adaptive?

Here is one of my not-so-superficial objections. The persuasiveness of the selection
metaphor gets extra clout from its link with the vague but pervasive concept of adap-
tiveness, which can supposedly be both created and preserved by natural selection. For
example, a book review insists that a particular piece of pedagogy be required reading
for non-Darwinist evolutionists who are trying to make sense of the world without the
relentless imperatives of natural selection and the adaptive trends it produces.12
Adaptiveness, as a quality of life that is useful, or competitively advantageous, can
always be applied in ways that seem to make sense. Even where adaptiveness seems
absent, there is confidence that adequate research will discover it. If equated with inte-
grativeness, adaptiveness is even a necessity of existence. The other day, one of my
students said to me: If it exists, it must have been selected. This has a pleasing
parsimony and finality, just like If it exists it must have been created. But it infers
that anything that exists must not only be adaptive but also must owe its existence to
natural selection. I responded: It doesnt follow that selection caused its existence,
and it might be truer to say to be selected it must first exist. A more complete answer
would have addressed the meaning of existence, but I avoid ontology during my
physiology course office hours.
Adaptive, unassuming and uncontroversial as it seems, has become a power
word that resists analysis while enforcing acceptance. Some selectionists compound
their logical burden by defining adaptiveness in terms of allelic fitness. But there are
sexually attractive features that expose their possessors to predation, and there are
Trojan genes that increase reproductive success but reduce physiological adaptabil-
ity.13 They may be the fittest in terms of their temporarily dominant numbers, but
detrimental in terms of ultimate persistence.
It is more logical to start with the qualities of evolutionary changes. They may be
detrimental or neutral. They may be generally advantageous (because they confer
adaptability), or they may be locally advantageous, depending on ecological circum-
stances. Natural selection is a consequence of advantageous or adaptive qualities.
Therefore, examination of the origin and nature of adaptive novelty comes closer to
the fundamental evolutionary problem. It is, however, legitimate to add that once the
novel adaptive feature comes into being, any variant that is more advantageous than
other variants survives differentiallyif under competition. Most biologists are
Darwinists to that extent, but evolutionary novelty is still missing from the causal
equation. Thus, with the reservation that some neutral or redundant qualities often
persist in Darwins struggle for existence, selection theory seems to offer a
reasonable way to look at what occurs after novelty has been generatedthat is, after
evolution has happened.
Oh, cry my student inquisitors, but the novelty to which you refer would be
meaningless if it were not for correlated and necessary novelties that natural selection
8 Introduction
had already preserved and maintained. So again I reiterate first principles: Self-
sustaining integrity, an ability to reproduce biologically, and hence evolvability were
inherent qualities of the first living organisms, and were prior to differential survival
and reproduction. They were not, even by the lights of extreme neo-Darwinists,
created by natural selection. And their persistence is fundamental to their nature. To
call such features adaptive, for the purpose of implying they were caused by natural
selection, is sophistry as well as circumlocution. Sadly, many biologists find it
persuasive. Ludwig von Bertalanffy (1952) lamented:
Like a Tibetan prayer wheel, Selection Theory murmurs untiringly: everything is useful, but as
to what actually happened and which lines evolution has actually followed, selection theory says
nothing, for the evolution is the product of chance, and therein obeys no law.14
In The Variation of Animals in Nature (1936), G. C. Robson and O. W. Richards

examined all the major known examples of evolution by natural selection, concluding
that none were sufficient to account for any significant taxonomic characters. Despite
the subsequent political success of ecological genetics, some adherents to the Modern
Synthesis are still puzzled by the fact that the defining characteristics of higher taxa
seem to be adaptively neutral. For example, adult echinoderms such as sea urchins are
radially symmetrical, i.e., they are round-bodied like sea anemones and jellyfish, and
lack a head that might point them in a particular direction. This shape would seem to
be less adaptive than the bilateral symmetry of most active marine animals, which are
elongated and have heads at the front that seem to know where they want to go.
Another puzzler: How is the six-leg body plan of insects, which existed before the
acquisition of wings, more or less adaptive than that of eight-legged spiders or ten-
legged lobsters? The distinguished neo-Darwinists Dobzhansky, Ayala, Stebbins, and
Valentine (1977) write:
This view is a radical deviation from the theory that evolutionary changes are governed by
natural selection. What is involved here is nothing less than one of the major unresolved
problems of evolutionary biology.15
The problem exists only for selectionists, and so they happily settle for the first
plausible selection pressure that occurs to them. But it could very well be that insect
and echinoderm and jellyfish body plans were simply novel complexities that were
consistent with organismal integritythey worked. There is no logical need for an
arbiter to judge them adaptive after the fact.
Some innovations result from coincidental interactions between formerly
independent systems. Natural selection can take no credit for their origin, their co-
existence, or their interaction. And some emergent novelties often involve redundant
features that persisted despite the culling hand of nature. Indeed, life depends on
redundancy to make evolutionary experiments. Initially selectionism strenuously
denies the existence of such events. When faced with the inevitable, it downplays
their importance in favor of selective adjustments necessary to make them more
viable. Behavior is yet another function that emphasizes the importance of the whole
organism, in contrast to whole populations. Consistent changes in behavior alter the
impact of the environment on the organism, and affect physiology and development.
In other words, the actions of plants or animals determine what are useful adaptations
and what are not. This cannot even be conceived from the abstract population gene
pools that neo-Darwinists emphasize.
If some evolutionists find it easier to understand the fate of evolutionary novelty
through the circumlocution of metaphorical forces, so be it. But when they invent
such creative forces to explain the origin of evolutionary change, they do no better
than Special Creationists or the proponents of Intelligent Design. Thus, the latter find
selectionists an easy target. Neo-Darwinist explanations, being predictive in
demographic terms, are certainly more scientific than those of the creationists. But
if those explanations are irrelevant to the fundamentals of evolution, their scientific
predictiveness is of no account.
What we really need to discover is how novelties are generated, how they integrate
with what already exists, and how new, more complex whole organisms can be greater
than the sums of their parts. Evolutionists who might agree that these are desirable
goals are only hindered by cant about the relentless imperatives of natural selection
and the adaptive trends it produces.
A Tradition of Re-invention
Natural selection has not always been regarded as an ever-present, omnipotent evolu-
tionary force. With regard to competition, Darwin himself inferred that after novelty
emerged there was a lag period before there developed a Ratio of Increase so high as
to lead to a Struggle for Life, and as a consequence to Natural Selection.16 A change
in form and function that allows novel exploitation of an existing environment, or
simply immigration into a pristine locality, permits occupation of empty niche
space. Experimentation with body forms has been described as the exploration of
morphospace.17 Implicit in these now-conventional concepts are adequate
resources, the ability to use them, and the absence of such agents of natural selection
as competition and predation. Differential reproduction is inevitable, but without
competition it might very well be random, not correlated with Darwinian fitness.
A proposal to re-invent natural selection may seem iconoclastically presumptuous,
but neo-Darwinists had no qualms about establishing a precedent when they
redefined it as differential survival and reproduction. While this addressed the effects of
the process, it left putative causal agents such as competition, predation, and the
literal choices that are made in reproductive pairing, and co-evolution, to be tacitly
implied. Natural selection is not simply the effect of evolutionary change, but a
syndrome of secondary causes and effects. As such, it is a real phenomenon, based in
some part on the participation of genes, and not to be abandoned for its creaky logic.
10 Introduction
To make matters worse, without a murmur of dissent from the orthodox, evolution
itself was re-invented as changes in the distribution of alleles in populations, for the sole
purpose of making it match the new definition of natural selection. What cloud of
unknowing allowed, and still allows, this to pass without protest? One answer is that
Darwin offered belief in natural selection as a mechanistic replacement for belief in
Special Creation. And stable belief systems characteristically tailor facts and
definitions to suit their acolytes and thus ensure their survival.
In Factors of Evolution (1949), Ivan Schmalhausen initiated the kind of reconceptu-
alization of natural selection that I consider necessary. What he calls stabilizing
selection is still a textbook cause of genetic equilibrium in populations. But most
accounts ignore the stabilization of internal organization, both developmental and
physiological, which was more important to him. Schmalhausen argued that such
adjustments reach an equilibrium that is difficult to escape, a condition most likely to
be reached in stable external environments. Yet he could see that the evolutionary
complexification of some higher vertebrates had paradoxically been accelerated. For
example, among the placental mammals, brain expansion had been faster than any
advances in the central nervous systems of the lower vertebrates. In the hominin
lineage, intelligence and mind had emerged even more rapidly. Schmalhausen could
not fully fathom how stabilizing selection had been thwarted, but he speculated that
stressful environments had something to do with it. The problem still confronts those
evolutionists who are awake to it.
Organisms under prevailing conditions of stable equilibrium are what I and most
other biologists investigate. Therefore, it is not surprising that this normal biology
should be given primary consideration in evolutionary studies, despite contradictions,
omissions, and paradoxes. Common sense also tells us that there is plenty of normal
biology to keep us grownups busy, so we should get on with it, stop asking sophomoric
questions, and quit worrying about the adequacy of the general theory. We can
depend on the high table18 of selectionism to send down theoretical crumbs,
predigested for easy absorption.
Those crumbs are devoid of essential nutrients. Selection theory actually says
nothing about the origin of the qualities that are selected. It only assesses them once
they have emerged, and predicts their likely distribution in future generations,
provided that the usual stability prevails. Evolutionary progress to organized
complexity is considered to be no more than a coincidental by-product of cumulative
adaptations, which very occasionally succeeds at beating the competition. Is there not
something distinctly unnatural about an evolutionary vision of nature that cannot
explain how innovation arises, does not see the need, and instead looks elsewhere to
observe how its consequences are played out? Re-invention is therefore a weak
response to these problems. Replacement is almost a necessity. But there are large
obstacles in the way.
Reductionism
Reduction is a good, logical tool for solving organismal problems by going down to
their molecular structure, or to physical properties. But reductionism is a philosophi-
cal stance that embraces the belief that physical or chemical explanations are
somehow superior to biological ones. Molecular biologists are inclined to reduce the
complexity of life to its simplest structures, and there abandon the quest. Selfish
genes in their gene pools are taken to be more important than organisms. To
compound the confusion, higher emergent functions such as intelligence and
conscious altruism are simplistically defined in such a way as to make them apply to
the lower levels. This is reminiscent of William Livants (1998) cure for baldness: You
simply shrink the head to the degree necessary for the remaining hair to cover the
entire patethe brain has to be shrunk as well, of course. This semantic reduction-
ism is rife in todays ultra-Darwinism, a shrunken mindset that regards evolution as
no more than the differential reproduction of genes.
Although reducing wholes to their parts can make them more understandable,
fascination with the parts makes it too easy to forget that they are only subunits with
no functional independence, whether in or out of the organism. It is their interactions
with higher levels of organization that are important. Nevertheless, populations of
individuals are commonly reduced to gene pools, meaning the totality of genes of the
interbreeding organisms. Originating as a mathematical convenience, the gene pool
acquired a life of its own, imbued with a higher reality than the organism. Because
genes mutated to form different alleles that could be subjected to natural selection, it
was the gene pool of the whole population that evolved.19 This argument was
protected by polemic that decried any reference to the whole organism as essentialis-
tic. Then came the notion that genes have a selfish nature. Even later, advances in
molecular biology, and propaganda for the human genome project, have allowed the
mistaken belief that there must be a gene for everything, and once the genes and their
protein products have been identified thats all we need to know. Instead, the
completion of the genome project has clearly informed us that knowing the genes in
their entirety tells us little about evolution. Yet biology still inhabits a genocentric
universe, and most of its intellectual energy and material resources are sucked in by
the black hole of reductionism at its center.
The Evolution of Whole Organisms
Because reductionism, whether as a simple bias or as an extreme prejudice, is the

dominant worldview, less attention is paid to the evolution of whole organisms. Is the
elaboration of all their complex structures based on the selective accumulation of
simple, randomly occurring adaptations at the gene level? In Darwins Black Box
12 Introduction
(1996), Michael Behe shows that molecular complexes often defy reductive analysis.
Then, without exploring mechanistic alternatives, he switches to his default cause: a
supernatural intelligent designer. This is the kind of argument from ignorance that
infests all the variants of creationism. In its place there should be a search for expla-
nations of how complexity can be integrated from multiple parts. Some complicated
organs seem to have been generated not only without any metaphorical selection
pressure, but even without any identifiable usefulness, far less any purposeful design.
For example, some jellyfish have image-forming eyes, but do not have the nervous
system needed to process visual images.20 One Darwinist responds:
The cubomedusan nervous system may be a black box at present, but sooner or later (God
willing) it will surely be found to have all the circuitry needed to process the information coming
in from those beady little eyes.21
However, a complex system might be elaborated, or simply fall into place like the
three-dimensional structure of a protein molecule, before there is a pre-existing need
for it, or another complex system to complement it, or a selection pressure to force it.
All experimental novelties in nature may emerge into such dubious conditions.
Life might be better understood if we took a step away from reductionism to deal
directly with the emergence and evolution of organismal wholeness. Most of us would
agree that an organism is more than a package of randomized alleles from the gene
pool, like a hand of cards from a well-shuffled pack. And it does not fly in the face of
convention to acknowledge that organismal uniqueness tends to be preserved from
generation to generation, despite genetic assortment, recombinations of parental
characters, and gene mutability. DNA analysis of the petrified remains of Cheddar
Man shows that some of his genomic integrity remains recognizable in one living
descendant, with no other close matches, despite 9,000 years of sexual mixing and
mutation.22 The structural dynamics of the genome as a whole are conserved from one
generation to the next by the behavior and architecture of chromosomes and meiotic
processes. At the species level, various obstacles to hybridization, such as geographical
separation, behavioral differences, and mutual sterility, prevent genetic mixing.
Within breeding populations there is a high probability that a particularly competitive
organismal uniqueness will persist and spread across the generation gap. But in reality
the genes themselves, despite rare exceptions in gene-transfer experiments, are
selflessly subordinate to the greater integrity of the whole organism.23
I call myself a realistic holist, meaning that I appreciate the necessity of under-
standing the parts in order to understand the whole, without adducing any
supernatural properties to the whole. A more neutral label has been popularized by
Susan Oyama in The Ontogeny of Information (1985). She uses interactionist to
describe someone who can work with wholes and parts without bias either way,
provided that their connectedness is taken into account. While this might be more
acceptable to someone who is on the road to recovery from reductionism, I still prefer
to advertise my bias toward the whole. To know how its integrity is maintained
requires that we understand the quality of adaptability. To understand how its
integrity is improved requires that we discover how adaptability evolves.
Adaptability
Adaptability is an emergent property of biological wholes. At its point of emergence

under normal stable conditions, this feature may not be seen to be for anything in
the short term; i.e., it need not realize any immediate reproductive improvement. But
if it had the tenacity to persist until it could break out of the bondage of competition,
or evade it by entering an environment hospitable only to its kind of adaptability, it
would then be free to diversify.
The organisms ability to sustain its integrity can be increased by evolutionary com-
plexification, whether or not it leads to immediate differential survival and
reproduction. Usually, increased complexity amounts to greater physiological and
behavioral adaptability, which decreases vulnerability to environmental changes and
the agents of natural selection. But this may be of little advantage in comparison with
established specialization in a stable environment. Other things being equal, self-
maintenance mechanisms are open to improvement through cumulative adjustments
of the new emergent condition that restore a dynamic stability within the organism.
But if internal adaptation comes to reinforce the status quo, how do further improve-
ments in adaptability get over that barrier? The simple answer is that they have to
jump over it or wait until it comes down spontaneously.
Ivan Schmalhausen argued that greater physiological and behavioral adaptability
promotes organismal diversification through the exploitation of stressful environ-
ments where competition, the main agent of natural selection, is weak or absent. In
contrast, although selectionism accepts the importance of unoccupied niches, it
proposes that they present a new assortment of strong selection pressures that induce
invading organisms to diversify. Although adaptability confers a blanket utility
responsive to numerous vicissitudes, neo-Darwinists do not recognize it as a necessary
qualification for invading new environments.24 They usually ignore it altogether or
bury it as an unexamined aspect of adaptation. Even so, however useful the adaptabil-
ity of emergent novelties might be under the confused conditions of invasion, it may
regress into specialization as new stable equilibria shake down.
The most likely response of a selectionist to these arguments would be: Admittedly,
there are occasions when adaptability may be important for survival. So thats what is
selected. Such a statement is true but irrelevant. There are often circumstances in
which adaptability is less important for reproductive success than a competitive spe-
cialization. But adaptability, as an emergent property of life, was not produced by
14 Introduction
natural selection, and it will not be entirely lost because of low scores in the selection
stakes. Moreover, as William Wimsatt (1998) has observed, greater complexity can
emerge autonomously from modular systems, and one does not need special circum-
stancesor selectionto form self-organizing states or properties: one needs special
circumstances to prevent them.25 It is essential that evolutionary theory discover how
complexity, adaptability and wholeness evolve, because they are what led ultimately
to the intelligence and freedom of thought that makes such a discovery possible.
Generative Hypotheses
The major operation of neo-Darwinist research is measuring the fitness of variants in

the real world of populations in their environments. The generation of novel
variants is still regarded with some indifference. Stephen Jay Gould remarks:
Speculation about adaptive significance is a favorite and surely entertaining ploy among evolu-
tionary biologists. But the question, What is it for? often diverts attention from the more
mundane but often more enlightening issue, How is it built?26
That leads us in to the even more enlightening question: how did it come to be built?
This question is difficult rather than mundanealways a popular reason to ignore a
problem. But if you accept evolution as a historical reality, and you are given to asking
naive questions, you may want to know how simple forms progressed to become
larger, more complex, and better organized. How did wholes as distinctive as horses
and tigers and trees evolve? If you are not content with answers that involve their
generation through DNA mutations that were marginally fitter than their ancestors,
if coincidental combinations in puddles of genes dont do it for you, or if you want
something more realistic than special creation or intelligent design, you may be
interested in my alternative:
During the course of progressive evolution, organisms have become more complex and
adaptable through a series of quite sudden, novel emergences.
They are produced by natural experiments, involving the interplay of environment,
organisms, internal milieux, developmental systems, and genomes. Large emergences can be
characterized as new wholes that are greater than the sums of their parts, with new properties
that did not exist at the lower level of their generative conditions, as well as their old features.
Metaphorically, the internal working of wholes may be fine-tuned by natural selection, and
fitter organisms will increase in number. But evolution is not caused by natural selection
neither metaphorically nor literally. Indeed, the whole syndrome of natural selection may
hinder the success of evolutionary experiments. Furthermore, even where better-adapted
variants seem to be directionally selected, they may be generated by autonomous, self-
amplifying, genomic mechanisms.
There are real (if rare) conditions of life in which the agents of natural selection are
diminished or absent and natures innovative experiments in emergent evolution have an
opportunity to thrive and diversify before their own numerical success reintroduces
competition. This happens in the wake of catastrophic changes, or when organisms invade
pristine environments, and on the rare occasions when novel emergents are so competent that
the old competition from pre-existing flora and fauna is irrelevant.
There are two major kinds of evolution. Once saltatory emergent progress has provided
increases in complexity, self-organization, and adaptability, i.e. progressive evolution, there is
greater potential for the second kind: diversifying evolution, which used to be called adaptive
radiation. Diversifying evolution itself has several major components. One is emergent,
producing epigenetic (developmental) changes, giving rise to specialized body forms through
allometric shiftswith behavioral consequences. The other is adaptational in the conven-
tional sense. It too has two manifestations: outwardly directed genetic adjustment to the
environment, and to habit.27 There is also internal co-adaptational adjustment to physiolog-
ical and developmental change, which may evolve regressions that are themselves saltatory.
Furthermore, if isolated lineages are founded by a small number of pioneers that share an
innovation, all of their descendents, including some from back-crosses with their pre-emergent
relatives, will possess their emergent properties from the outset. Invoking natural selection as
a means of spreading innovation through the population may be superfluous.
For those who do not find selectionism sufficient, an examination of the origins of
progressive emergent qualities might make a welcome change. Of all the ideas with
which I challenge my students, they usually accept this: The causal theory of evolution
has to include a hypothesis that suggests how innovation is generated. Darwin and his
descendants have not formulated a generative synthesis. Their hypothesis only
circumscribes the demographic fate of novelties.
Generative hypotheses are needed not only for adaptational mechanisms that fit
organisms to particular conditions of life, but also for processes of progressive (i.e.,
complexifying) innovation. Since these usually have the emergent property of
universal advantage through more sustainable integrity or adaptability at their
inception, they need no subsequent sponsorship by natural selection. Regardless of
present and future circumstances, their persistence is assured, though not necessarily
as the fittest types. Here the concept of selection verges on total redundancy. Indeed,
if you look at the generation of any novelty, adaptable or adaptational, as the primary
process, you can see that, barring accidents, its future depends on its quality. To add
the subsequent action of a directing selective process is logically superfluousif you
are dealt a handful of aces, the outcome of the game is certain from the start.
Emergent innovation might proffer increased complexity, and multifunctional
adaptability. It might involve divergences in behavior and in developmental
pathways, novel additions to the life cycle, and allometric shifts in anatomical
16 Introduction
proportions, as occurred in the evolution of a giraffe from a short-necked okapi-like

ancestor. Adaptational advantage in the environment into which it is born is another
possibility. Or it might fail in any of those offices. If chance is discounted, the fate of
a novelty, in terms of its ultimate differential survival and reproduction, is contained
in its origin, much as the physical fate of the universe was contained in the initial
conditions of the Big Bang.28 Though natural selection qua differential reproduction is
always present, it is an effect, not a cause.
What difference would it have made to the history of biology if someone before
Darwin had come up with a generative theory of evolution, in which the concept of
selection was no more than a means of describing, quantifying, and cataloguing the
ultimate fate of primary causal events? Obviously not much, since we find something
like it in On Generation, an essay published by Erasmus Darwin (grandfather of
Charles) in his 1794 book Zoonomia. Lamarck also had a generative theory, according
to which an inherent progressive drive caused evolution, and adaptation to particular
environments through the inheritance of acquired characteristics was a lesser process
that sometimes got in the way. Twenty-six years before the publication of Charles
Darwins major book, tienne Geoffroy de St. Hilaire tried to explain the origin of
species using those exact words to define the problem. He concentrated on how
environment could generate developmental monstrosities that could be advanta-
geous or detrimental. But he took no account of relative competitiveness.
Erasmus Darwin did not make his point strongly enough to persuade an unprepared
readership. Lamarckism failed because most biologists intuitively realized that
universal progress was wrong. Like Lamarck, Geoffroy was a victim of Cuviers anti-
evolutionary antagonism. As a result, the baby generative theory was thrown out with
the dirty bathwater of progressionism. Lamarcks theory would have had a better start
in life if he had made evolution a series of occasional random events. The neo-
Lamarckists moved in that direction, and they might have pulled off a paradigmatic
coup had Darwin not already established a strong alternative worldview, with natural
selection the sine qua non of evolution. Innovations, however they occurred, were only
raw material to be shaped by his mechanism.
What Are the Options?
The re-invention of natural selection as an obstacle rather than a cause, or simply as a

consequence of the generation of novelty, would leave the neo-Darwinist Modern
Synthesis of evolution with little foundation. Would it need renovation, or a new
structure? Postmodernists want to abandon the ruins as a memorial to authoritarian-
ism, and substitute a tent village of refugee concepts for the old monolithic paradigm.
I prefer something more constructive.
A dialectical approach to evolutionary causation might take natural selection as the
thesis. Something else, such as the epigenetic origin of novel complexity, might be the
antithesis. Several evo-devos (developmental evolutionists) are hoping for such a

new synthesis. But it would be too narrow, ignoring physiological and behavioral
adaptability and the major emergences that resulted from symbiosis. Some theoreti-
cians relegate natural selection to a secondary though essential process that is the
consequence of a primary mechanism of their choosing. Other dissidents try to save
their skins by calling on natural selection as a final arbiter that eliminates any
organism suffering from disintegrative change. But this is a spurious role for selection;
failure is self-interring, and a funeral undertaker is redundant.
To imagine that these compromises provide any freedom of thought from neo-
Darwinism is a delusion that recalls the Buddhist parable about Monkey. Trying to
escape the hand of Buddha (Darwin being cast here in Buddhas role), Monkey ran and
ran to the ends of the Earth, where he found an enormous pillar at the brink of the
bottomless abyss. Thinking that Buddha could not rule from so far away, and that he
might rule there himself, he carved his name on the pillar and returned to claim
success. Buddha then displayed the finger with Monkey inscribed on it. To effect his
escape, Evolutionary Monkey must dwell at the edge of the abyss, and contemplate its
traverse, without constantly running back to Darwin for approval.
Progressive Evolution
If natural selection is taken to be an obstacle to progressive evolution (in the sense of
increased self-organizing complexity), a start from scratch, beyond the mortemain of
Darwin, is demanded. When asked If you are going to reject natural selection as the
cause of evolution, what are you going to put in its place? I am tempted to answer
that selection theory has never offered a logical generative theory of progressive
evolution, so there is nothing that requires replacement. But to be less of a dog in the
manger, I suggest that what causes innovative variation causes evolution, and that
these phenomena, though sometimes elusive, are natural events that happen within
the organism as well as without.
The word progress has two strikes against it, even in modern discussions of
evolution. Strike one stems from Lamarcks belief that evolution was progressionistic,
meaning that an inherent, inexorable trend continuously made organisms more
complex. This was immediately tainted by his adduction of spontaneous generation
to explain how a multitude of organisms had reached lower states of complexity than
others. Lamarck was forced to conclude that their ancestors of simple living organisms
must have spontaneously originated later than those of complex organisms.
Lamarckist implications about progress still arouse suspicions that that evolutionary
form is deterministici.e., that there is some kind of trend that has been bound to
result in self-awareness in one lineage or another. But its determinism-quotient
diminishes with the realization that progress is not inexorable but random, episodic,
terminable, and indeed reversible. Strike two against the word progress is its sense of
18 Introduction
human betterment. Evolution was long identified with human progress in the
industrial and economic realms, with division of labor, and with increasing social
organization. This notion was strongly held by Erasmus Darwin. His grandson Charles
believed that evolutionary progress, like economic progress, required that the compet-
itively superior had to prevail and the inferior had to die out. The evolution of
something better clashes with modern biologists self-proclaimed objectivity. And
they regard progressive evolution as a reification of woolly thinking about inherent
trends.
However, there is nothing mysterious or even disputatious about a process of pro-
gressive evolution if it is taken to be the equivalent of increasing complexity of
self-organization. Progressive evolution arises from the fundamental replicative
quality of life. Where there is reproduction, it is inevitable that organisms, and the
building blocks that make them up, must multiply. Where there is multiplication, dif-
ferentiation is inevitable in some cases, since a replication mechanism that is flexible
enough to operate in a living organism must also be mutable. A biological system
consisting of multiple, differentiated modules has the capacity to integrate
innovations, if it has hierarchical regulation. Since regulatory processes themselves,
such as modifier gene action, and hormonal and nervous mechanisms, can also
multiply and differentiate, they can keep pace with the other complexities. If self-
organization is an idea that bothers you, just remember that you began as a single cell.
You had more than a little help from your mother, but the rest was by your own self-
organization. The genes were some of the parts that came with your assembly kit, but
were not the instruction manual.
Emergent wholes can become more complex simply by having a greater variety of
parts. In some, the universal building blocks will fall into new structural and
functional configurations that exhibit greater order, which implies greater energetic
economy and which results in prolonged persistence of the system. For example, a
two-dimensional sheet of cells can spontaneously form a more stable three-
dimensional sphere under turbulent conditions. Such spontaneous complexification
of the organism has the potential to improve the maintenance of integrity through
adaptability. The result is wider scope for experiments in diversification. They may
work, or they may fail. If they work they may wear out, but survival of biological
experiments is furthered by making new copies of complete, functioning organisms.
Thus, the unique and fundamental emergent property of life is persistence of
its autonomous, complex patterns through adaptability and reproduction. To
conclude that there has been a trend for some lineages (our own, for example) to
evolve to greater complexity is a subjective historical interpretation. Complexification
certainly occurred, but it is more objective to think in terms of the occasional and
somewhat unpredictable realization of potentials under the appropriate generative
conditions.
There is nothing new about these ideas. Hermann J. Muller, one of the first fruit-fly
geneticists, proposed in 1926 that since chromosomal material could duplicate, occa-
sionally mutate, and reduplicate in the changed form, evolution would happen
automatically. But his audience thought he was joking.29 In the same vein, he later
wrote: If selection could somehow be dispensed with, so that all variants survived
and multiplied, the higher forms would nevertheless have arisen.30 Mullers higher
forms had the price of admission to a new environment, not as a specific pre-
adaptation to a specific element, but as pre-existing adaptability. Also, if the newcomer
was to diversify morphologically, it needed a plasticity not found in organisms whose
development had been rigidly canalized. A generative theory is needed to account for
the origin, nature, and evolution of adaptability and plasticity. Selection theory only
quantifies their consequences.
There is much more to it than the complexification of autonomous self-
organization. Occasionally, major emergent biological changes in the organism are
caused by the acquisition of genetic material from foreign sources. Among the earliest
prokaryotes, gene-swapping across phyletic lines seems to have been the norm. Recent
advances in the human genome project have revealed the relatively recent acquisition
of bacterial genes. In the case of the endosymbioses that gave rise to the eukaryotic
cell, whole new genomes were acquired, organisms and all. In addition, the
environment can induce physical, physiological, and behavioral changes in the
organism that continue to be felt by subsequent generations before becoming
genetically assimilated. Disruption of the environmentlocal or universal, slow or
cataclysmicis also a major influence on evolution. There is nothing mysterious
about these causes either, and the Modern Synthesis of conventional evolutionary
theory is attempting to subsume some of them in yet another layer of ad hoc
hypotheses. But I am going to rearrange these pieces of the evolutionary puzzle and
take more than a few liberties with the current rules.
Metaphors
In biology, metaphors are commonly used as a substitute for inclusive definitions of
complex processes or ideas. Since everybody likes to discuss the causes of evolution in
figurative terms like natural selection, selection pressure, and survival of the fittest, it
should not be too confusing if I give a little more weight to the common expression
natural experiment.31 Darwin himself thought in terms of a self-improving
industrial workshop.32 But instead of the research and development side, he
emphasized the process of competition that decided which of the workshops new
products were to survive. Therefore, over the long haul I will be more concerned with
the primary, generative causes of evolution than with re-inventing Darwins
metaphors. Natural selection, however defined, would not occur in the absence of
natural experiments in variation. On the other hand, natural experiments are
conducted independently of natural selection.
20 Introduction
Breakthrough experiment extends the metaphor. Any invention can be so distinc-

tively and immediately successful as to be universally accepted and applied. Or it may
be a mere curiosity that barely registers until a theoretically or technically useful
application is found. Natural experiments, or emergences, may have to wait for the
right conditions. At that point their emergent properties become belatedly obvious
because their numbers increase. In a few cases, natural breakthrough experiments will
simultaneously meet the tests of qualitative novelty and improved integrity, giving
them the opportunity to multiply, either in competition with existent types or in a
new environment free of competition.
The natural experiment metaphor is more than mere word play. In Evolutionary
Theory: The Unfinished Synthesis (1985), I remarked that the concept could be extended
to genetic engineering: if it works in the lab, why not in nature?33 Just about then, a
particularly appropriate exemplifying technique was developed. Agrobacterium
tumefaciens is able to insert a plasmid into host plant cells that modifies their products
in its favor, and this natural, bacterial, genetic engineering mechanism was co-opted
by molecular biologists to introduce foreign genestransgenesinto plants.34 Of
course, in a natural experiment earlier in its evolutionary history, Agrobacterium had
acquired plasmid genes from a primitive plant host. The natural experiment with
plasmids was in place before its consequences in nature or in genetic engineering were
played out. These parallels between nature and the genetics laboratory lead logically
to contemplation of how common complicated natural experiments might be, how
they are field tested, and if and how nature clears the bench to conduct a new series.
Related questions include the following: How fast are natural experiments? How long
do their field tests take? Is the experimental laboratory in constant or only occasional
production?
The Rate and the Gait of Evolution

On the face of it, evolution has taken more than 3 billion yearslong enough to
reassure the most conservative gradualists. Indeed, their credulity is tested by such a
long passage of time. For example, it is a regular procedure to average to a constant
rate the number of gene mutations that have become characteristic of species over
geological time. But selectionists admit that the averaged rate may have been too slow
to respond to relatively quick changes in selection pressure. That evolution is episodic
is not too radical an alternative. Moreover, if molecular processes are essential to evo-
lutionary change, it might even be heuristic to think of the speed of evolution on the
same scale as the speed of chemical reactions. Most of the time is spent in stasis, with
experimental mutations mostly undone by repair mechanisms or shut out by
normalizing selection. But suppose that real innovative evolution is packed into a
series of brief spurtsmere moments of biological time. To persist, such experiments
need freedom from the major agents of natural selection. Then erratic molecular
changes can be fixed as fast as they come, until dynamic stability is re-established.
Unfortunately, molecular biologists who accept episodic evolution think it is caused
by intensification of selection pressure.
Those who accept the Big Bang theory believe that all the cosmic criteria that were
to determine the universes future were established in the first fraction of a second.
The fastest physicochemical transitions in complex organic molecules are measured in
microseconds. Biochemical reactions establish the ground of evolutionary change in
milliseconds; their physiological consequences occur in seconds; their epigenetic
results unfold in a few months. The complete experimental reproductive cycle and
feedback between environment and organism may take little longer. A geological time
scale may be needed only to account for the prolonged obstruction of progressive evolution by
stases that are reinforced by natural selection.
Is this the principle of punctuated equilibrium reduced to absurdity? Am I looking
at reality through the wrong end of the telescope? If that is what you think, remember
that punctuated equilibrium has never been exposed to such a philosophical test. Its
proponents still talk about punctuations as being rapid on time scales of tens of
thousands of years. As to looking through the wrong end of the telescope, the
compound microscope was discovered by doing just that, and figuratively speaking we
need both kinds of instrument to analyze natures evolutionary experiments.
There is more to my proposition than a downgraded natural selection and an
pumped-up punctuationism. As an alternative to the Modern Synthesis, I suggest that
we work toward an Emergence Theory that accounts for generative mechanisms and
the emergent qualities of their evolutionary products. Although it exists at this stage
of my argument only as a framework proposal, I will put together a compendium of
examples of evolutionary emergences with a variety of causes, along with some
working hypotheses. Although I have been drawn to emergence theory by research
into comparative physiology, functional anatomy, and symbiosis, it is not cut from
the whole cloth of my own speculations. Neither the basic concept nor the name is
new. The problem of the generation of order from disorder was debated by Aristotle
and his contemporaries. Although not evolutionists, they wondered how humans
could develop from chaotic vital fluids. Erasmus Darwin, Lamarck, and Geoffroy
proffered generative theories, and other biologists have long recognized the need for
one.
A Generative Emergence Theory
In 1923, Conwy Lloyd Morgan published Emergent Evolution. Its implications were
appreciated by some of his contemporaries, and for a while it affected evolutionists.
But the attention of biology was diverted by the success of neo-Darwinism and subse-
quently by the reductive analysis of DNA. A vague sense of emergence nevertheless
22 Introduction
continues to permeate evolutionary writing. Selectionists themselves distinguish

emergent, key innovations from minor adaptational changes. Complexity theorists
attempt to explain and quantify how emergent order is generated in simple systems.
A unifying matrix is still needed for all the causal biological components of emergence
to complement each other as a new synthetic whole.
Conventional wisdom acknowledges that some revolutionary events in biological
evolution have potentiated far greater diversification than others. These are the great
emergences: rapid, unpredictable, progressive changes that brought life into existence
and have on occasion radically altered the course of its history, passing beyond the
boundaries of old restraints, and constructing new levels of existence, relatedness, and
operation. Such natural breakthrough experiments have not always exploded into
diversification. Instead they often have had to wait for existing stases to be disequili-
brated. Since they are relatively rare, neo-Darwinism ignores them, assuming them to
be fortuitous consequences of the normal activity of natural selection. But they
present too many awkward imponderables to conform nicely to selection theory.
The word emergence implies a process of radical evolutionary change, and it is
rich in synonyms that apply to coming out of water onto land, to hatching from an
egg, to a secret truth revealed, and to human cultures undergoing fundamental
change. Because many biologists appreciate the need for explanations of evolutionary
emergence, and have an intuitive grasp of the concepts necessary to understand them,
it may now be easier to find a receptive audience than in Morgans day.
John Maynard Smith and Eors Szathmry have addressed a variety of important
emergences in The Major Transitions in Evolution (1995). They enter most of the
significant causal arenas, and examine the processes in some detail, despite an explicit
selectionist bias:
The transitions must be explained in terms of immediate selective advantage to replicators. We

are committed to the gene-centred approach outlined by Williams [Adaptation and Natural
Selection, 1966] and made still more explicit by Dawkins [The Selfish Gene, 1976].35
Venturing into unexplained phenomena that most of their fellow ultra-Darwinists

have ignored as irrelevant to the real stuff of evolution, they break down the major
transitions to intermediate steps that have a clear advantage over the more primitive
stages. But they do not explain how the steps were generated. Moreover they admit
that paradoxical situations must have existed for which it is difficult to imagine what
that the selective advantage might have been, and they invoke undefined special cir-
cumstances to explain those situations away.36 My goal is to expound, not explain
away, the special circumstances of emergent evolution.
There are two ways to proceed. In Emergence: From Chaos to Order (1998), John
Holland takes the low road, from the bottom up. This parsimonious approach to the
analysis of emergence starts out from simple mathematical models and extrapolates
toward higher-order emergences. As an organismal biologist, I take the high road,

from the top down.37 I examine familiar structural and functional diversities, not to
see what they are for, but to see how they are built and how they might have
originated. To make the numerous examples less confusing, I sort them out into the
major arenas of evolutionary performance, and try to find common features of
causation that together might make up an Emergence Synthesis.
The theory that evolution really happenedthe historical or phenomenal
theorywas supported by evidence presented by Darwin in The Origin of Species. It is
partially independent of the causal theory, which deals with the mechanism of
evolution. But new evidence and new ideas about the saltatory nature of complexifi-
cation challenge Darwins interpretation of the history of life, as well as the causal
theory. In the context of emergence they certainly call into question the Darwinian
and neo-Darwinist views of evolution as a gradual, insensible, continuous, adapta-
tional process.
In Unpredicted factors of evolution: The theory of emergence re-visited (1985), I
suggested that emergentism could provide an epistemological framework for the con-
struction of a comprehensive alternative to the Modern Synthesis. I could have played
it safe by leaving natural selection alone and simply presenting emergence as a
synthesis of generative principles that are needed to fill the present gap in evolution-
ary thought. This is what Brian Goodwin asks for in his 1989 essay Evolution and the
generative order. Then, in How the Leopard Changed Its Spots (1994), Goodwin simply
ignores natural selection and begins to expand on generative principles as a Science of
Qualities.
Whether ignored or taken to be irrelevant to the generation of novelty, the
framework of selection theory remains a valid mathematical system for dealing with
any demographic consequences of evolutionary change. In addition, quantified
fitness gives clues to the biological significance of emergent features. Nevertheless, the
need for a generative synthesis becomes more obvious if the role and the limitations
of natural selection are reappraised. Historically, selectionism has obstructed the
development of generative theories by asserting that natural selection is the all-
sufficient cause of evolution, and that the Modern Synthesis amounts to an
all-sufficient theory of evolution that subsumes generative causation. Therefore,
dismantling this barrier is more than an attention-getting defiance of convention. I
also wish to make my intentions clear from the outset, instead of sailing under false
colors and hoisting the Jolly Roger in the last chapter. But the re-invention of natural
selection is an opening salvo, not my overall strategy.
A fledgling emergence theory or synthesis would have to try its wings as the kind of
unifying compilation that Julian Huxley provided in Evolution: The Modern Synthesis
(1942). Although it would fly in the faces of both modernists and postmodernists, it
is needed to address the fundamental nature of evolution and its mechanisms. It
24 Introduction
would present evolutionary history as a mixture of rapid saltations (progressive and

regressive) and sudden changes that appear at critical points in continuous processes.
Some of its elements are broadly predictable; others are contingent on physicochemi-
cal and biotic conditions. Natural experiment is the art of the possible, and
successful emergences, where they have the freedom to do so, result in bursts of diver-
sification, interspersed with long periods of stasis.38
A full-fledged emergence theory would distinguish between adaptability and
adaptation, profoundly different features of life that have always been lumped
together in neo-Darwinism. Furthermore, speciation, which is pivotal for Darwinian
evolution, would be seen primarily as a ratchet pin that prevents evolutionary cogs
from slipping. Finally, emergentism could release biology from the genocentric
universe in which it is confined and restore it to one in which whole organisms and
their interactions are the stars of the biological and ontological fundament.
Conclusion
Natural selection has already had just about had all the re-invention it needs, even
from those who support it as a primary cause of evolution. Its supporters understand
that the causes of variation are independent of natural selection, and occasionally
they hint that natural selection might even get in the way. George Williams (1966)
admits:
Mutation is of course, a necessary precondition to continued evolutionary change. So evolution

takes place, not so much because of natural selection, but to a large degree, in spite of it.39
What the supporters of natural selection dont understand is that they have now
minimized the importance of natural selection as a causal explanation of evolution.
And the next step is to see it as a barrier to the success of natures experiments. Once
the obscuring cloud of selectionism is removed, evolutionary innovation can more
easily be worked into a general thesis. There is plenty of raw material from which a
generative thesis can be constructed. It has been accumulating ever since the
publication of Origin, despiteand often in open defiance ofselectionism. The
essential message to keep in mind during the preliminaries is that we need to pay more
attention to evolutionary origins and less to their fate.
However, despite everything I have said about the limitations, obstructions, and
obfuscations of selection theory, the fact remains that most of the history of life has
been dominated by dynamic stabilities imposed by the syndrome of effects and
agents circumscribed by the term natural selection. The most general biological
synthesis must take this into account. Therefore, although clearing the decks of
obstructive clutter is immediately necessary for positive action, getting to the right
destination is the larger goal. Once I have dealt with the causal arenas of progressive
evolution and assembled an emergence thesis, I will reintegrate that thesis with a
selectionist antithesis in chapter 11.
Before proceeding to the substance of emergence, I extend my critique of selection-
ism in chapter 1. Then, in pursuit of evolutionary origins, I advance an argument and
evidence in favor of a reincarnated emergentism, beginning with chapter 2 (a primer
for several chapters on the causal arenas of emergent evolution) and continuing with
three chapters on more theoretical aspects.
As well as acknowledging relevant hypotheses and discoveries of modern biologists,
I try to rehabilitate mute, inglorious historical contributions. Modern biology is
often compromised by their omission. Molecular biologists in particular seem to think
that the Big Bang of Biology came in 1953, with the Watson-Crick model of DNA,
and that only post-millennial research now matters.
1
Paradigm Drift
In the past 30 years or so, ultra-Darwinians have reformulated their basic conception of natural
selection, changing it from a passive to a directly active agent operating in the natural world,
pushing the evolutionary process relentlessly forward. . . . They seek to transform natural
selection from a simple form of record keeping, a filter that biases the distribution of genes
between populations, to a more dynamic active force that molds and shapes organic form as time
goes by.
Niles Eldredge, 19951
If natural selection is the filter, whats making the coffee?

Camilla Berry, 20002
Like Darwin, many biologists would admit that the creative power of natural selection
is metaphorical. Like Eldredge, they might see it only as a passive filter for genomic
variations. But Darwin also promoted it as a power incessantly ready for actionan
instant substitute for the supernatural creator.3 If he had not, his version of evolution-
ary theory might not have caught on in the first place. But only a fractured logic could
simultaneously make a metaphor into a materialistic force, hedge on it as a false
term, and yet endow it with Biblical creativity: What limits can be put to this power,
acting during long ages and rigidly scrutinizing the whole constitution, structure and
habits of each creature,favouring the good and rejecting the bad?4 Natural selection
has always been a dualistic principle: metaphorically active and mechanistically
passive. Is Eldredge right to infer that the re-invention of Darwin has involved a
qualitative, paradigm shift, to the point where natural selection is perceived to make
the coffee as well as filter it? In this chapter I will raise my objections to natural
selection in both those roles.
I will presume that most of my readers consider that natural selection is the cause
of evolution, and that selection theory therefore makes sense. What makes it
difficult to argue otherwise is that natural selection is not only the foundation of the
modern mechanistic theory of evolution, it is also a real phenomenon. As such, it is
28 Chapter 1
an aspect of life, and what it makes sense of is not evolution but population
dynamics. It is therefore irrelevant as a causal explanation of evolutionary change. I
do not reject the real phenomena pertaining to the syndrome of natural selection.
They are what dominates life most of the time.
The demographic causes and effects addressed by selection theory will be merged
with emergence theory to form a new Biological Synthesis in chapter 11. Also, be
assured that I am aware of the perils of writing about a new synthesis or a new
theory when such labels are commonly stuck on propositions that are neither.
Paradigms
Paradigm is a word that slipped into fashionable parlance before being explicitly
understood by all who used it. Many philosophers are still dubious about its meaning
and significance. Now favored by advertising copywriters, it teeters on the brink of
banality. But the concept of a novel theory that generates a period of new experimen-
tation and theorizing has enduring value for the history of ideas.
There are two kinds of paradigm in science. One arises from a significant
phenomenon that is either newly discovered or newly recognized as a mechanistic
entity, hence constituting a phenomenal paradigm. The second, a causal paradigm,
arises from the purported explanation of an accepted phenomenon. It is the one that
causes most of the arguments. The discovery of a natural phenomenon, whether it be
gravity, electricity, the cell, germs that cause disease, or evolution, has a paradigmatic
influence in its early years until its reality is taken for granted. Thereafter it need
undergo no further revolutionary reinterpretation unless the original data are found
to have been false or misinterpreted. For example, before the inception of Cell Theory
it had long been recognized that plant tissues are composed of cells, because their
cellulose walls are visible under simple microscopes. Then, in 1839, Schwann
proposed that animal tissues were also cellular. This unifying theory of the
microanatomy of living organisms took hold as a paradigm that gave direction to the
study of embryology, chromosome behavior, biochemistry, and gene theory. Since
these could relate cellular structures and functions to whole organisms, cell theory was
a successful reduction that influenced biology for the next century. The cellular
condition itself became axiomatic and uncontroversial.5
A paradigm need have little foundation in fact to be universally persuasive. Take
eighteenth-century Fiber Theory, for instance. As a physiological and medical
paradigm, it did not directly address evolution, but it illustrates a significant general
principle. Dominating medicine for about a hundred years, Fiber Theory proposed
that all organisms were made up of fluid humors and elastic fibers, whose tension was
an indication of health. Friction, fermentation, viscosity, blocked pores, and corrosion
by acids, alkalis, and oxygen all could cause fevers. Therapy involved bloodletting to
Paradigm Drift 29
balance the humors and tone the fibers. The fiber paradigm succeeded because it
combined the ancient, traditional humoral theory, which had sanctioned universal
therapeutic bleeding, with contemporary scientific knowledge of physics, chemistry,
and the microanatomy of circulation. It inspired Erasmus Darwin to consider that all
living forms might have evolved from a primordial fiber that differentiated according
to changes in its immediate environment. Lamarck thought that the pressure of subtle
humors could alter anatomy. And in Frankenstein (1818), Mary Shelley imagined that
the vivification of the body fibers by electricity could resurrect a cadaver. To displace
the fiber paradigm, the combined assault of Cell Theory and the Germ Theory of
Disease was needed.
The Modern Synthesis of evolution has this much in common with Fiber Theory: it
combines diehard tradition and cutting-edge technology. The two paradigms also
involve phenomena that are real, but irrelevant to the major paradigmatic premise.
Friction heats, and oxygen corrodes, but fever and inflammation are effects of disease,
not its causes. If the same logic is applied to Selection Theory, differential reproduc-
tion is real, but it is an effect of evolution, not its cause. Fortunately, although the
Modern Synthesis is as flawed as Fiber Theory, it has practiced only metaphorical
bloodletting.
Evolutionary Paradigms
Biological paradigms require individual, pragmatic treatment, since their conception
and development have not followed a simple formula. Also, evolutionary paradigms,
which attempt to establish universal biological principles, fail to obey the strict
definitions demanded by some philosophers of science.6 As a general rule, any
paradigm, worldview, or school of thought that has irrational componentsthat is, all
of themcannot be scientifically cut and dried. Evolutionary theory has not lurched
from one revolution to another in the way that Thomas Kuhn portrayed the
paradigms of physics in The Structure of Scientific Revolutions (1962). Instead, the evo-
lutionary paradigm just keeps on absorbing and expanding and forgetting where its
been.7
The first extensive evolutionary theory was put forth in Lamarcks La philosophie
zoologique, published in 1809, the year Darwin was born. Although it made a splash
when it was launched, it was anything but watertight. The inheritance of acquired
characteristics was not the contentious issue it is now. But Lamarcks exposition of the
process and mechanisms of evolution, such as spontaneous generation, universal evo-
lutionary progress, and the idea that organisms actively responded to needs, had no
scientific basis. Nevertheless, despite his errors, and the misrepresentations of his
critics, Lamarck brought evolution to the center of attention. Many accepted that
evolution might be a reality, even if Lamarck was wrong about the nature of the
process and its mechanisms.
30 Chapter 1
The Darwinian Paradigm

The launch of Darwins flagship theory was successful for reasons other than its
originality of design and soundness of bottom. Evolution and the mechanisms of
natural selection and adaptation had already been widely discussed by numerous
biologists. But by working things out for himself, Darwin brought fresh insight to
them. His dogged persistence was supported by influential friends, who assisted with
the publication of The Origin of Species. It was immediately boosted by T. H. Huxley,
who, after years of digging in his heels on evolutionism, became Darwins bulldog.
Before any development of a general theory of evolution, taxonomists had also
helped to prepare the way for it with their systems of classification. In particular, the
systematics of Linnaeus suggested natural evolutionary relationships. The concept of
a distinct species that was closely related to others within its genus was a powerful
referent for all of biology, and its applied arts. Therefore to explain the origin of species
was something that everybody already felt to be important, and it was the mainstay
of Darwinism. Darwins readers could agree that horticulturists and animal breeders
had produced distinct plant and animal strains. It followed logically that in the
natural world the trend toward varieties could proceed further, to new species, and
from there to the evolution of higher taxa. From a common ancestor, a diversity of
species adapted to different environments could arise, and this adaptive radiation
dovetailed neatly with the familiar concept of homology. Darwin thus had an
audience of prepared minds.
By making evolution progress fitfully through random changes in only a few
lineages, instead of through a universal drive to perfection, Darwin disarmed the
objections of materialists like Huxley, and then impressed them with his evidence for
the historical reality of evolution. The concept of natural selection, a working
hypothesis rather than an experimentally established theory, was good enough for the
time being. Moreover, Darwin rounded off the Age of Enlightenment nicely by
replacing divine law with natural law. These factors cooperated to elevate Darwinism
to paradigm status, and some modern biologists think that no further revolution is
necessary. The phenomenal reality of evolution has been established, despite some dif-
ficulties with its definition. What is still open to debate is a causal paradigm built on
the proposition that natural selection causes evolution.
Survival of the fittest was a concept familiar to ancient hunters, farmers, and
philosophers. But it had not previously led to the concept of evolution. That had
instead grown out of pre-evolutionary systematics, nature philosophy, speculation
about the mutability of species, and paleontological discoveries. But by giving the
historical theory substance and form, Darwin positioned his mechanistic causal
hypothesis strongly. Moreover, since his historical evidence included the effects of
artificial selection, he could link evolution with the analogous mechanism of natural
selection. Before The Origin of Species, no one had amalgamated the two ideas so
Paradigm Drift 31
persuasively. For Darwin, evolution had to be through modification by natural

selection. Phenomenon and cause were entwined so intricately that the one could not
exist without the otheraccepting the existence of evolution required the acceptance
of natural selection as its cause. When Special Creationists argue that evolution must
be rejected if natural selection is shown to be an unsatisfactory cause, they are only
applying Darwinian logic.
For Darwinists, it took no leap of faith to see that species varied in the makeup of
their individual members. Variants that were better adapted, or more fit for the
prevailing conditions of life, would be most successful at reproducing their character-
istics and passing them on to subsequent generations. It was as if a metaphorical
breeder were selecting some for reproduction, and rejecting less desirable forms from
the broodstock. Metaphorical agents, used incautiously, can be reified into tangible
forces, and lose touch with reality. Nevertheless, it is evident that some features of
organisms in nature are biologically superior to others, and consequently survive and
reproduce more successfully. This aspect of Darwinism is so self-evident that it makes
sense to everybody. That it makes no sense as an explanation of how the superior
features were generated in the first place doesnt seem to be self-evident, since few
notice the omission.
The historical elements of Darwinism have been refined and occasionally jostled by
molecular biology, but the reality of evolution has never been in dispute within
biology. At first the very idea caused a stir, and debate focused on its plausibility and
on the adequacy of the causal explanation. Evolutions affront to fundamentalist
Christian dogma has resurrected the same debate in every subsequent generation, but
within biology the theory that evolution consisted of real historical events soon
ceased to have a central paradigmatic role. It was the causal hypotheses that became
controversial.
Neo-Lamarckism and the Rise of Neo-Darwinism

By 1882, the year of Darwins death, neo-Lamarckism was making the running as a
new evolutionary synthesis. In addition to most of the original Lamarckian laws, neo-
Lamarckism proposed that the environment imposed direct heritable changes on
organisms. It also included natural selection. However, its role was to cull unfit
variations, since the environment could cause detrimental as well as advantageous
changes. Lamarcks sense of inherent universal progress in nature was missing from
neo-Lamarckism. For many neo-Lamarckists, especially E. D. Cope, and William
Bateson in his early neo-Lamarckist phase, developmental evolution was especially
important. This gave them the intuition that evolution was discontinuous, whereas
Lamarck thought it was gradual. The appeal of something for everybody,
the traditional allied with the contemporary, is always a strong combination. It
therefore competed successfully with the revised Darwinism proposed by the first
32 Chapter 1
neo-Darwinist, August Weismann, who had pledged to purge evolutionary theory of

everything except the all-sufficient mechanism of natural selection.
In 1908, the English grandfather of ultra-Darwinism, E. B. Poulton, delivered a tub-
thumping manifesto that also proclaimed natural selection as the one true cause. He
denounced not only neo-Lamarckism, but also the revisionism of Weismann and the
biometricians, who had tried to out-Darwin Darwin. For Poulton, the generation of
the novel qualities from which natural selection chooses was quite unimportant: So
long as individual variation is present, so long as it is hereditary, it does not signify
how it is produced. . . . So long as it is there it is available, and Natural Selection can
make use of it.8 No generative theory for Poulton: to insist that the origin of variation
had any importance was the revolt of the clay against the potter. Darwinists and
neo-Darwinists have substituted one imaginary creator after another for the supernat-
ural one: an architect for Darwin, a potter for Poulton, a sculptor for Mayr, a blind
watchmaker for Dawkins. All of them ignore generative hypotheses to give natural
selection the creative role.
Despite Poulton, Darwinism was partially eclipsed by neo-Lamarckism, by Hugo De
Vriess Mutation Theory, and by William Batesons neo-Mendelism in the first decade
of the twentieth century. But supporters of these ideas were quickly reconverted. T. H.
Morgans Drosophila work began to pull him back from mutationism to gradualistic
Darwinism and Mendelian genetics. Then, for his book Mimicry in Butterflies (1915),
the entomologist R. C. Punnett, a close associate of Bateson, commissioned the math-
ematician H. T. J. Norton to construct a set of tables that would theoretically predict
the effect of a slight selective superiority in a variation. Punnett, a saltationist at heart,
was surprised when Norton showed that the smallest advantage would spread rapidly
until it dominated the population. For the time being, the lid was nailed down on the
coffin of mutation pressure. Selection pressure came to the fore.
Why had mutation pressure seemed so important? Previously, the Darwinian idea
that heritable characters of the parents are blended in the offspring was widely
believed. This would have made it impossible for any small novelty of variation to
sustain its distinct nature for long, because of homogenization with the more
common characters. The only hypothetical solution for this problem was to assume
that any novelties had to be saltations or large-scale mutations. The Mendelian
demonstration that hereditary traits did not disappear through blending inheritance,
combined with Nortons calculation that characters with small selective advantages
would rapidly spread in populations, made saltations theoretically unnecessary
much to the relief of Darwinists who shared their masters concern that they made
selection redundant. This did not alter the fact that, as Darwin pointed out, mon-
strosities often appeared spontaneously, especially in domesticated organisms.
The question of how variation arose, regardless of its evolutionary potential, began
to be answered by chromosome theory. It also clarified the role of sexual reproduction,
Paradigm Drift 33
which involves random exchanges of homologous chromosomal material, leading to

recombination (mixing of parental features). Even in organisms with only a few
chromosomes, there is an astronomical number of possible combinations, most of
which are viable and available as raw material for natural selection. To this source of
variation the modern concept of mutation can be added. When the structure of DNA
was discovered, it was realized that point mutations (alterations in the sequence of
bases in the DNA code) could bring about changes in the proteins into which the code
was translated. Here, so it seemed, was the missing explanation of the origin of
variations needed for natural selection to do its stuff.
A new wave of neo-Darwinism rose in the 1930s from theoretical population
genetics, which quantified fitness and selection, and predicted the genetic, and
demographic make up of future generations. Since there will be no subsequent need
to bring up Weismanns first wave, I will apply neo-Darwinism to the later phase. Its
supporters knew that old-fashioned Darwinism had been taking a beating. They were
determined to mend it, and to turn their new version into the dominating force of
evolutionary biology.
Neo-Darwinist Semantics
One of the reasons for the momentum of neo-Darwinism was its revision of
definitions of natural selection and evolution.
Neo-Darwinist Natural Selection

Neo-Darwinists knew that Darwins synonym for natural selection, survival of the
fittest, came down to no more than survival of those that survive. Therefore, they
redefined natural selection as differential survival and reproduction. Differential
referred to the relative success of variants at evading or improving predation and
beating the competition.
Fitness denoted the degree of adaptation to environment in Darwinian theory,
and under neo-Darwinism it simply expressed the numerical distribution of particular
variants as percentages, the most numerous being classed as the fittest. As such it is
clear and uncontroversial. Refinement of the concept has vitiated the circularity of
the survival of those that survive. But circularity remains; it has simply become dif-
ferential reproduction of those that differentially reproduce. In the first glow of
righteousness, neo-Darwinists pretended not to notice that differential survival and
reproduction are effects and not causes. Natural selection is really the result of an
aggregate of interactive causes, including competition (intraspecific and interspecific),
predation on animals, and browsing on plants. In addition, there are sexual selection
and the types of co-evolution in which the literal choice of one organism by another
influences reproductive success. Relative resistance to disease and to climatic change
are also qualities that result in differential reproduction. It may seem odd that a cause
34 Chapter 1
should be defined in terms of its effect, without reference to its agents, but selection-
ists claim that the tacit agents add up to an integrating explanation.9
Regardless of its awkward logic, natural selection, qua differential survival and repro-
duction, makes sense because it is a real and ubiquitous phenomenon. But these
features do not automatically make it causala brook always has a babble, but the
babble does not cause the brook. Nor does any definition of natural selection contain
an explanation of what Cope called the origin of the fittest, referring to the source
of novelty, the raw material that natural selection refines.10
However, selection theory provides a rough inductive guide to emergent evolution.
By counting alleles, a notion of the quality of evolutionary novelty can be indirectly
reached, although distorted by the conditions of life that prevail at the moment.
Those conditions are usually a state of dynamic equilibrium, and so neo-Darwinism
has always concentrated on the stability of populations. As population biologists
readily admit, natural selection is largely a normalizing or stabilizing process that
operates for a large number of generations without shifting the distribution curve, far
less ever producing a new species. Under most circumstances, minor change, or simply
no change, usually is the best way to stay in the game. The evolutionary stable
strategy, a concept introduced to population biology from game theory by John
Maynard Smith (1978), should realistically be called non-evolutionary stable
strategy, since it describes how change is resisted in the presence of strong
competition.
Competition is nevertheless believed to be a significant factor that can carry
a lineage out of stasis through directional selection. It supposedly leads to the differ-
ential survival of exaggerated features that give a competitive edge. In evolutionary
arms races, predation pressure is believed to be more important than competition.
The preys protective armor, size, or evasive skills become enhanced, and the predators
armor-piercing claws and teeth, strength, size, and speed are improved. Since
competition and predation cannot literally direct appropriate genetic change, their
random mutation and selection may not be the mechanisms involved in biological
arms races. Directional evolution could result from narrow epigenetic constraints, or
a more fundamental process of genetic self-amplification.
More interesting are occasions when competition and predation are absent.
Contrary to the notion that evolution cannot occur under such circumstances, natural
experimentation occurs anytime and anywhere, without immediate reference to
natural selection. And some emergent types might need freedom from competition
and predation to find their feet (or roots). Conventional selectionism makes much of
how immigrants to isolated islands evolve rapidly, and here absence of competition
and predation is important. The same conditions apply when environments have
been cleared by some natural disaster. On rare occasions, under non-catastrophic cir-
cumstances, existing competition may become irrelevant if a newly emergent
Paradigm Drift 35
phenomenon is immediately superior. Business entrepreneurs, often social Darwinists,

use the saltatory expression getting the jump on the competition. But conventional
Darwinism has evolutionary change occur in insensible steps, to allow natural
selection to always be in control. And in new environments, new, strong selection
pressures hurry things alonggradually, but a bit less gradually than usual.
Selection Pressure
At the top of this chapter I asked if Niles Eldredge is right in saying that there has been
a qualitative shift to an ultra-Darwinism that makes natural selection a force that
actively generates adaptation. For me, quantitative shifts are more significant. One
symptom of neo-Darwinist extremism is a greatly increased emphasis on the creativity
of selection pressure. It infests the writing of even the most reflective neo-Darwinists.
The metaphor of a pressure that eliminated inferior varieties was originally used by
Alfred Russel Wallace in his Ternate essay, published as part of the Darwin and Wallace
papers by the Linnean Society in 1858:
Now, let some alteration of physical conditions occur in the districta long period of drought, a
destruction of vegetation by locusts, the irruption of some new carnivorous animal seeking
pastures newany change in fact tending to render existence more difficult to the species in
question, and tasking its utmost powers to avoid complete extermination; it is evident that, of
all the individuals composing the species, those forming the least numerous and most feebly
organized variety would suffer first, and, were the pressure severe, must soon become extinct.11
[emphasis added]
An interesting contrast is found in the way Ivan Schmalhausen used pressure in

Factors of Evolution: The Theory of Stabilizing Selection (1949). He wrote about the vital
energy of the organism (as a representative of a definite species), or its pressure upon
the surrounding environment as leading to natural selection.12 This pressure tended
to be constant under stable conditions, but could increase for particular types when
conditions changed. Although Schmalhausen used neo-Darwinist language, and also
thought in terms of aggressive repression of organisms by extreme environmental
conditions, it is clear that he saw that generative evolutionary pressures were to be
found in organisms, and the effects were to be found in natural selection.
Unfortunately, neo-Darwinists were to take from Schmalhausen only what they barely
needed to understand stable populations, and find the selection pressure is all they
needed to do. Selection pressure is now given a metaphorically creative sense by
modern biologists. Although there are many superficial instances of such adaptations,
there are many other instances of appropriate adaptations that could result from only
the slightest genetic change, and yet such adaptations have not appeared.
To understand the problems with selection pressure and response to need, consider
this example: Female grassfinches are attracted to males with artificial crests, so there
36 Chapter 1
must be an almost tangible, strong selection pressure for natural crests. Unfortunately,
conceiving how female predilection for sexy head gear can suck a crest of feathers out
of a male grassfinchs head is rather difficult. Nothing of the kind has in fact appeared
naturally in any of the 120 species of grassfinch, although it is a common condition
in many of its passerine relatives. There are many cases where the slightest nudge to
an existing genotype could bring out advantageous traits. But the nudge has not been
nudged, or the traits have refused to appear.13
In Chance and Necessity (1971), Jacques Monod equated necessity with selective
pressure. Necessity drives the selection of chance events in the direction of
adaptations appropriate to the particular habits and habitat of the organism. To his
credit, Monod recognized that logically this is no different from Lamarcks scorned
Second Law, which proposed that organisms evolved in response to their needs. A
creative selection pressure is not only superfluous, it is logically the same as Lamarcks
proposal that organisms respond to needs. Lamarck made the organism the agent of
evolutionnot an imaginary external force. In every generation, neo-Darwinists flog
the dead horse of Lamarckism; but instead of punishing Lamarck for his Second Law,
they ought to be flagellating themselves for selection pressure. In any case, the physic-
ochemical and biotic environment can have a direct causal influence: it changes the
internal nature of organisms, shapes their development, influences their behavior, and
occasionally offers freedom from the usual agents of natural selection. Under such
conditions, the expression selection vacuum or negative selection pressure would
be more appropriate.
Neo-Darwinist Evolution
To complement their new definition of natural selection, neo-Darwinists redefined
evolution as changes in the distribution of alleles in populations. This premise does
not even require stable mutations of alleles. Existing alleles can change in their distri-
bution from generation to generation through differential survival and reproduction
without the slightest progressive evolutionary or directional effect. The new definition
of evolution also opened the door to random, non-selective events like genetic drift,
which resulted in increased numbers of alleles that did not have the highest fitness.
Then along came the neutral theory of molecular evolution, which argued that the
numerical distribution of alleles was not a reflection of natural selection. Lucky breaks
such as bottleneck effect and founder effect involve random subsampling of the parental
population. Although founder effect is regarded as a key to diversification in island
populations, such non-selective events are regarded as insignificant special cases of
evolution.
Epistemologists have always upheld the Hippocratic aphorism that an adequate
hypothesis should save the appearances, or account for all of the known manifesta-
Paradigm Drift 37
tions of the phenomenon in question. And yet the progressive or complexifying

component of evolution is missing from selectionist formulae. To avoid argument,
some selectionists say that increase in complexity is epiphenomenala possible but
rare cumulative by-product of the action of natural selection. However, George
Williams takes a harder line:
I would maintain . . . that there is nothing in the basic structure of the theory of natural selection
that would suggest the idea of any kind of cumulative process. . . . Gene substitution would
slightly improve the precision of one or more adaptations, but as perfection is approached the
opportunity for further improvement would correspondingly diminish. This is not a process for
which the term progress would be at all appropriate.14
Perfection yes; progress no? For Williams, organisms that seem to have progressed to
higher forms and functions are simply better adapted under some circumstances. He
insists, moreover, that organization should only be used in that context:
When a biologist says that a system is organized, he should mean organized for genetic survival
or for some subordinate goal that contributes to successful reproduction.15
The slighting of progress has been rationalized by others on the grounds that it is too
burdened with political economics to be worth retaining. Others say that evolution-
ary history needs to be kept apart from its causation for the sake of clarity. But the real
reason for ignoring the issue is that neo-Darwinism cant explain it. And there is this
underlying dread: What if complexification is autoevolutionary and irrelevant to
selective advantage?
Neo-Darwinist Adaptationism
In the introduction, I discussed the elusive semantics of the innocent word adaptive
and said that it becomes even more slippery when innovation that is adaptable or
adaptational is said to be elicited by selection pressure. Whatever evolution wants,
and can get, it does get.16 Stephen Jay Gould and Richard Lewontin (1979) say that
such adaptationism is Panglossian, after Voltaires character who said that
everything happens for the best. Under such critical fire, the theoretical elite come out
from behind their Looking Glass, where evolution gets what it wants, and where
natural selection makes what it wants, to regroup under the flag of formal definition.
But soon they retreat back through the mirror, proliferating more preposterous circu-
larities such as wings are adaptations to flight or eyes are adaptations to sightas
if flight and sight were metaphysical absolutes that existed before the emergence of
wings and eyes.
Fuzzy logic is a necessary part of tentative thought experiments, but it should not
continue to be used so vaguely into the maturity of a theory. Indeed the language of
neo-Darwinism is so careless that the words divine plan can be substituted for
selection pressure in any popular work in the biological literature without the
38 Chapter 1
slightest disruption in the logical flow of argument. Little wonder creationists find it
such an easy mark. But they and selectionists have this in common: faith in the
efficacy of a creative mechanism that has no material reality. Theological
Darwinians have accepted Darwins view of natural selection as a secular creator.17
And throughout their writings there is now no straightforward evolution; it has
acquired a fixed epithet as evolution-through-natural-selection. These semantic re-
inventions of Darwinism and neo-Darwinism contributed to the polemical success of
the Modern Synthesis.
The Modern Synthesis
During the second and third decades of the twentieth century, hypotheses and
opinions were shifting from saltationism back to gradualism. But the Darwinian
paradigm would have lost steerage way if it had not been for popularizing works that
brought theoretical population genetics into a general evolutionary context. The
Causes of Evolution (1932) by J. B. S. Haldane was first to serve this purpose. Setting out
to rescue Darwinism, Haldane discussed the likelihood of evolution happening faster
in isolated populations, and suggested the importance of developmental genetics.
Theodosius Dobzhanskys Genetics and the Origin of Species (1937) broadened the
treatment of evolution through genetic change, and catalyzed a more comprehensive
amalgamation of evolutionary disciplines that was to take its name from Julian
Huxleys Evolution: The Modern Synthesis (1942). Ernst Mayrs Systematics and the Origin
of Species (1942) is another component of the founding corpus of the Modern
Synthesis, along with G. G. Simpsons Tempo and Mode in Evolution (1944), which
merged neo-Darwinism with paleontology. Bernhardt Renschs Evolution above the
Species Level argued that the same process that caused speciation caused evolution at
the highest taxonomic levels. First published in German in 1947, it was embraced by
the Modern Synthesis when it came out in English translation in 1959, because it
made microevolution all-sufficient.
American evolutionists and textbooks often ignore Julian Huxleys role in the
development of the Modern Synthesis. Ernst Mayr (1980) credits Huxley with the
introductory application of the word synthesis and notes that he had often
discussed it with him. But he remarks that Huxley was luckier than the other
pretenders because he published first. Frederick Churchill (1980) considers Evolution:
The Modern Synthesis as little more than an expansion of a conference address delivered
by Huxley in 1936, and politely refers to the last chapter on progress as curious,
although it was central to Huxleys synthesis. William Provine (1988) regards Huxley
as a compiler, rather than a synthesizer. He notes, incidentally, that not only Huxley
felt left out by the Americanized Modern Synthesis; almost every ego connected with
evolutionary biology in the 1940s, whether in Britain or America, felt injured. Niles
Paradigm Drift 39
Eldredges The Unfinished Synthesis (1985) argues that the Modern Synthesis made even
paleontology walk the plank, only to be reluctantly invited back to dine at the
captains table in the last decade or so. But he ignores Huxley. By a curious coincidence
of metaphor, my Evolutionary Theory: The Unfinished Synthesis was also published in
1985. In it, I took a dim view of the various forms of the Modern Synthesis, and was
already looking for a comprehensive theory that would reject the neo-Darwinist
excesses that were already developing. Since then, I have acquired a better apprecia-
tion of Huxleys attempts to deal with progressive evolution.
Jeffrey Schwartz (1999) describes Glenn Jepsens account of how W. H. Bucher first
mentioned a synthesis of genetics, morphology and paleontology in 1941. Then
Columbia University incubated the idea that further discussions at formal meetings
would let the protosynthetists learn each others languages. It hatched at a major
conference in 1947, whose proceedings were published in 1949 as Genetics,
Paleontology and Evolution, with the credit going to Jepsen, Mayr, and Simpson.18 Most
of this happened after Huxley published the book that popularized the usage of the
term synthesis and gave it a more comprehensive treatment than any of its
subsequent rivals. Why is Huxley so ignored? Michael Ruse (1996) says that although
prodding from Huxley helped formalize the synthesis in America, he was sidelined
for being too much of a progressionist.19 Also, other evolutionists were not too happy
about allometry and embryological evolution since they smacked of orthogenesis and
saltation. And there was one additional niggling worry about Huxley:
Huxleys intentions were synthetic, and synthesizing is precisely where he succeeded, as never
before. Yet . . . there was something of his grandfather about his approach to evolution. There
was a part of Huxley that was never that deeply committed to adaptationism.20
Many biological studies had been developed independently of evolutionary theory.

Huxley meant to integrate all of them, using progress, or what some of his contempo-
raries were calling macroevolution, as the unifying theme. I am persuaded by Ruse
that Huxley was disreputable among the synthetists because he was not enough of a
selectionist, and by Mayrs (1980) inference that Huxley was too soft on orthogenesis,
allometry, and progress. But I hesitate to exclude pure American chauvinism as a
reason for dropping Huxley. In any event, the priority that American synthetists gave
to quantitative neo-Darwinism was to subsume all the rest. Their version of the
synthesis may have reduced conflicts between different specialists, and may have
given them the sense of a common cause, but it also shed some of the important evo-
lutionary causes.
The most comprehensive and detailed general account of the development of the
Huxleyan and American versions of the Modern Synthesis is proffered by Vassiliki
Betty Smocovitis in Unifying Biology: The Evolutionary Synthesis and Evolutionary Biology
(1996). Since it is not in her mandate to evaluate the biological foundation of the
40 Chapter 1
Modern Synthesis, Smocovitis sees selection theory as a positive part of the slow
unification of biology. To her, the American version was more cohesive through the
frequent interaction of its contributors, and Huxleys monograph was relatively disor-
ganized, though appealing to a wider audience outside biology. She does, however,
acknowledge William Provines judgment that the American Modern Synthesis is
easier to define in terms of what it rejected than what it synthesized.21
Let us take a break to consider how the word synthesis has been used by evolu-
tionists. It may mean little more than an amalgamation of independent studies that
provides encyclopedic convenience. A unifying synthesis may harmonize a
disjointed discipline with the application of an integrating explanation, a role
awarded to natural selection in the Modern Synthesis. Furthermore, if independent
investigators come together to actively examine fields with which they were once
unfamiliar, there is a good possibility that novel hypotheses will emerge from a fusion
of previously isolated ideas.
The dialectical synthesis of thesis and antithesis is another alternative. Applied
effectively it might produce a powerful new theory. As well as resolving contradic-
tions, it involves the heuristic association of independent concepts. Julian Huxley,
though familiar with the genre, gave no hint that he had such a purpose. However,
Ernst Mayr (1980) argues that the new synthesis was the fusion of two independent
and sometimes conflicting research traditions: experimental genetics and population
studies. Both sides benefited from their new insights, so the whole was now greater
than the sum of its parts. Such an event, Mayr adds, occurs only occasionally in the
history of science.22 As to the situation prior to the synthesis, he writes:
I am appalled at the misunderstandings, the hostility, and the intolerance of the opponents. Both
sides display a feeling of superiority over their opponents who simply do not understand what
the facts and issues are. How could they have ever come together? Just as in the case of warring
nations, intermediaries were needed, evolutionists who were able to remove misunderstandings
and to build bridges between hierarchical levels. These bridge builders were the real architects of
the synthesis.23
Thus Mayr elevates the Modern Synthesis beyond the attempted unification of Huxley
(who gets an honorable mention as a bridge builderwe are left to guess who the
primary engineer of this rare, momentous synthesis might be). Mayrs interdiscipli-
nary bisociation end runs the kind of Kuhnian revolutionary interpretation that he
finds distasteful (Mayr 1972). But it sails close to a dialectical synthesis.
Scientific syntheses of this kind have no automatic claim to righteousness. The
bogus Fiber Theory was also an invigorating fusion of two research traditions. For any
kind of synthesis, all the arguments need to be aired, and awkward exceptions
confronted at the outset instead of being black-boxed, ignored, or liquidated. The
Modern Synthesis has failed this test, and has lost many of the comprehensive features
Paradigm Drift 41
that Huxley gave it. No amount of historical revisionism can make up for that. Yet it
persists, and it can still beat the competition.
Paradigms Lost?24
Three quasi-paradigms were lost when neo-Darwinism came to the fore. One was neo-
Lamarckism. Another was Hugo De Vriess Mutation Theory, supported by William
Batesons neo-Mendelism. A decade or so later, a flash-in-the-pan version of
emergentism suffered the same fate. What these had in common was saltatory
evolution, but the early brand of emergentism also suffered from associations with
mysticism. The gradualistic and materialistic Modern Synthesis has held sway ever
since, aground though it might be. What might it take to finally blow it off its reef?
In The Structure of Scientific Revolutions (second edition, 1970), Thomas Kuhn
suggests a new paradigm may be imminent when the existing one is in a state of crisis,
as marked by several signatures. First, there is the failure of the old paradigm to
explain new data:
The profession can no longer evade anomalies that subvert the existing tradition of scientific
practise. . . . Then begin the extraordinary investigations that lead the profession at last to a new
set of commitments, a new basis for the practise of science.25
Darwinism and its descendants have postponed crisis by going with the flow of
changing ideas, and then ignoring the anomalies, or subsuming them into its thesis.
But what of other indicators? Kuhn (1970) writes:
Because it demands large scale paradigm destruction and major shifts in the problems and
techniques of normal science, the emergence of new theories is generally preceded by a period of
pronounced professional insecurity. As one might expect, that insecurity is generated by the
persistent failure of the puzzles of normal science to come out as they should.26
If this is so, selection theory, which has been confronted by crisis for a quarter of a
century, shows remarkable paradigmatic fitness. Biologists can retreat to their many
professional niches, and conduct much of their research without reference to the
central theory. Maybe they see no profit in participating in a vituperative ongoing
debatename calling and righteous indignation should be added to Kuhns signatures
of crisis. Those who feel insecure want to accept the reassurances of reliable
authorities, who, in turn, oblige by deploying an array of sophistries to meet this end.
In the mess of the Modern Synthesis, the evolutionary elite at the captains table keep
beating the selection gong.27 The dictum that ideas grow old and die with their
originators does not apply: new evolutionary authorities with more extreme versions
of the same old ideas have grabbed the vacant privileged seats. At the captains table,
accommodation of any previously antithetical idea, referred to as change of
emphasis, is accompanied by rounds of self-congratulation for the vitality of the
42 Chapter 1
evolutionary debate. However, the reverberating extremism of ultra-Darwinism might

yet disequilibrate the paradigm enough to give emergent ideas a chance to be
established. Kuhn further comments:
In periods of acknowledged crisis scientists have turned to philosophical analysis as a device for
unlocking the riddles of their field. The search for assumptions can be an effective way to weaken
the grip of a tradition on the mind and to suggest the basis for a new one. Scientists have not
generally wanted or needed to be philosophers. Indeed normal science usually holds creative
philosophy at arms length.28
Simply quoting Kuhn is philosophical commentary, and The Structure of Scientific

Revolutions is still one of the most frequently cited books in the scientific literature. It
is also the Bible of the postmodernist flotilla that tries to blockade biological
modernism. They declare that dominant paradigms tend to treat relative truths as
absolute. Therefore they should be cut down, and new ones should be nipped in the
bud, lest they too repeat the errors of the past. At best we should be allowed to choose
from a fleet of alternative models.29 Biological postmodernism came in with structural-
ism and the New Biology of the 1970s and 1980s, but its attack on evolutionary
modernism seems to have left selectionism intact. Have these assaults weakened the
Modern Synthesis at all? If so, how close might it be to breaking up?
In The Darwinian Revolution (1959), Gertrude Himmelfarb pointed out that
Darwinists and their successors avoided confrontations by subsuming antitheses
under the conventional thesis. Awkward contradictions were simply filed as special
cases and then forgotten. Some were flatly judged wrong and ignored. But if antitheses
are constantly subsumed, a thesis is likely to list and go off its original course; indeed
the drift of the original paradigm would have revived Darwins chronic seasickness.
Given a glimpse of twentieth-century perspective, Darwin would certainly have been
relieved at the retention of natural selection as the cause of evolution. But he might
have wondered why the organism had been marooned while population thinking,
selfish genes, and molecular reductionism had been taken on board. Neo-Darwinism
started out on the purposeful course of quantifying population theory, which seemed
to give it the same kind of predictive powers as physical laws. However, it had
provided nothing qualitatively new by the time it signed on with the Modern
Synthesis. Under this name the superstructure was rebuilt and extra cargo embarked,
but, already aground, it could go nowhere, and a lot of special cases, ad hoc
hypotheses, and other flotsam and jetsam have drifted up against it ever since.
The Modern Synthesis retains the same kind of appeal that neo-Lamarckism had a
century ago: something to offer everybody, provided they accept natural selection as
the ultimate cause. Sometimes it is credited with the active role of discovery, investi-
gation, and analysis of antithetical phenomena. The following quotation is from a
popular introductory biology textbook:
Paradigm Drift 43
The modern synthesis recognizes, and in fact first described how other mechanisms such as
genetic drift and chromosomal mutations can cause rapid, nonadaptive evolution. But the major
emphasis of the synthesis is on gradualism and natural selection.30
This sinks below historical inaccuracy. Not only does it reify the synthesis as an agent
of investigation, it falsely infers that apparently antithetical phenomena were
discovered through its inductive guidance. The anti-Darwinist Richard Goldschmidt,
who promoted the saltatory causal role of chromosomal mutation and position
effects, would turn in his graveif he has ever stopped spinning since his interment.
Furthermore, it shows how little improvement there has been in the 40 years since
Himmelfarbs admonition. An antithetical discovery about rapid evolution is
subsumed and toweled over with gradualism and natural selection. The captains
table responds that the language may be loose and figurative, but everybody knows
fundamentally what is going on. The evidence is to the contrary. Most non-biologists
who accept neo-Darwinism, as well as many orthodox biologists, seem to think
entirely in figurative terms: Natural selection and selection pressures are real driving
forces of evolution. Every generation of undergraduates is brainwashed into this way
of thinkingIf it exists, it must have been selected. Biology is constantly being mis-
represented to students and the public at large, and only an arrogant elite with serious
vested interests would connive at that.
Some adherents to the Modern Synthesis are not completely stifled by it. In one of
the most forthright treatments of the subject, Natural Selection in the Wild (1986), John
Endler issues standing orders that ought to be nailed to the mainmast of the Modern
Synthesis:
Natural selection is a process which results from biological differences among individuals, and
which may give rise to genetic change or evolution; it is not a force that acts, and does not
have an intensity. By analogy with a chemical reaction process, natural selection has a rate and
rate coefficients, which are estimated by fitnesses. The same analogy shows why force is an
improper analogy: it is not a force that causes the change in reactant frequencies, but the
chemical properties of the reactants.31
Endlers analogy tells us to find the properties of the generative reactants that give rise
to emergences. Identifying them with individual genes is not enough, because gene
expression is instructed by higher levels in the organismal and environmental
hierarchies.
One difficulty in dealing with selection theory, as Endler sees it, arises from the
kinds of logical confusion that I have just described. He does a fair job of clearing it
up. It helps that he even considers natural selection as a result of differences, which for
me translates as natural selection is the effectas opposed to the causeof evolu-
tionary change. More explicitly, he states that origins of evolutionary novelties are
external to the selectionist program of causation. Endler also cautions the faithful that
44 Chapter 1
natural selection is not easy to detect. Lack of detection of it, when present, is
compounded with apparent detection when it is absent, and with misleading demon-
strations of its existence.32 If these points too were highlighted in orders of the day for
the Modern Synthesis, the paradigm might not be stuck so fast on a reef.
It is one thing to regret the minor deficiencies of the Modern Synthesis as its
supporters see them, or to reminisce over the loss of the neo-Lamarckist,
mutationist/Mendelist, and emergentist pretenders. It is entirely another to consider
what the Modern Synthesis has rejected. Here a keening chorus will not do. Those
aspects of the evolution of life must be reinstated.
The Loss of Life, Organism, Mind, and Evolution
If the most enlightened analyst replaced Pangloss at the helm, the flagship of the
Modern Synthesis would still be on the reef where neo-Darwinism put it, with no
ability to maneuver, only to sit there and accumulate more ad hocsam and jetsam,
ignoring inadequacies and subsuming serious contradictions as special cases of the
neo-Darwinist thesis. The Modern Synthesis had no dialectical agenda for the future
accommodation of antithetical ideas so as to advance to a new synthesis. It made
complete castaways of neo-Lamarckism, and direct effects of environment, and it
neglected developmental evolution. Simpson was browbeaten into renouncing his
earlier flirtation with orthogenesis, and megaevolutionwhich, after all, came down
to the abhorrent saltatory progress (what Mayr calls soft evolution). Unification of
the synthesis was gained by losing evolution and replacing it with changes in the dis-
tribution of alleles in populations.
When population thinking came along, the Modern Synthesis lost the organism as
well. At the time it was necessary to correct a common misapprehension about
evolution. Novelties spring from the germ lines of parents without appearing in the
parental phenotypes. In the next generation these novelties are manifested phenotyp-
ically, but the individual organisms do not evolve. Or do they? Their own actions
affect them and future generations. For example the nutritional health of the mother
may influence the condition of her ova, and their subsequent development. Exposure
to extremes of stress may directly increase the mutability of DNA and change
methylation patterns. So what is the way round this paradox? What actually evolves?
According to population thinkers, if there is random mating and gene flow in a
population, then the entire population pool of genes is available to produce the
subsamples that constitute organisms. Moreover, since individuals do not possess all
of the genetic characteristics of the whole population, a comprehensive account of
evolution must involve the entire gene pool, not the organismal bits. The population
supposedly evolves by changing the numerical proportions of existing alleles and by
incorporating novel alleles with high selective value. Another conventional reason to
Paradigm Drift 45
emphasize populations is that they persist for long enough to have evolutionary clout;
individual plants and animals are too ephemeral.
In Phenotypes (1994), David Rollo gives the issue more focus by writing that it is
phenotypic lineages within populations that are selected and evolve. Moreover, for
him, lineage evolution involves a lot more than allele redistribution and structural
gene mutations. Progressive factors like improvement in developmental, physiological
and behavioral organization are important. And he gives whole individual phenotypes
active evolutionary roles that affect the fate of the lineage. All I need say differently
for the moment is that lineages do evolve, but selection qua differential survival and
reproduction is a consequence of the qualities of those lineages, not a causal agent. And
no matter how much better one lineage is than another, it will finally establish its
own change-resistant equilibrium.
Individual organisms began to be ousted from any evolutionary consideration
because pools of genes are easier to work with statistically, and behave less aberrantly.
As a consequence, evolutionists who thought that there was more to a population or
an organismal whole than the sum of its genes were dismissed as Platonic essentialists.
A similar criticism was applied to anyone who thought an archetypal individual could
found a new lineage, since the whole gene pool had to be seen as the real foundation.
Plato had remarked that what we perceive of nature is a corruption of its true essence,
as if we were observers in a cave, looking at the shadows of beings that passed outside.
But it seems to me that the gene pool is the shadow play. Population thinkers have
transferred the essence of the organism to the populationnot a population of actual
creatures interacting with each other in a real environment, but a mathematical model
devoid of life.
Individual genes have also had essences transferred to them. Genes are all that
matter to molecular biologists because genes are what they study. It should not be
surprising that they inflate reductionism out of egotism. But to help shift biology to
the genocentric universe a rogue singularity was needed. It arrived in the form of the
selfish gene. As originally conceived, it only cooperates with others to reach the goal of
replication, and uses organisms merely as transportation mechanisms.33 Such
romantic reductionism, combined with the genes-for-everything hyperbole of
genomics, has greatly appealed to simplistic materialists, and to the current crew of
sociobiological anthropologists and evolutionary psychologists on the ultra-
Darwinism watch. If behavior and even mind are gene-determined they are susceptible
to natural selection, and the modernist program is served. This logic should not be
surprising eitherin earlier rejecting higher and lower we had already lost our
minds.34
The phenomenon of life itself is also secondary to natural selection. Vitality has too
many bothersome, essentialistic, ineffable qualities, and the conventional stance
infers that it must merely be the arithmetical sum of the functional parts of a living
46 Chapter 1
organism. Survival and reproduction have been inherent features of life since it first
emerged. But in the reversed Looking Glass perspective of selectionists they are the
products of natural selection. When challenged, revolving-door logic whirls them out
from behind the mirror to the reality of differential survival and reproduction.
If it exists it must have been selected has an ontological contradiction that Darwin
intuitively distinguished when he equated physiological adaptability with the innate,
wide flexibility of constitution that allowed an organism to persist in its own
being.35 Spinoza, who called the essential quality of persistence conatus, wrote:
The endeavour with which each thing strives to persist in its own being is nothing
else than the real essence of that thing.36 Darwins exclusion of natural selection as
the agent of persistence in being is significant. Since he did not pursue the idea
further, he probably realized that it undermined his own major premise, and like
much of Darwiniana it has been ignored by the Modern Synthesis.
Persistence in being, flexibility of constitution, adaptability, self-organization, and
homeostasis are all aspects of the integrity of the organism that can be dealt with inde-
pendently of special physiological and ecological exigencies. Adaptabilities that
preserve integrity are to be found at any level from the molecular to the behavioral in
an organism, and they extend out into its ecosystem. Lamarck implied that they
evolved progressively and were distinct from adaptational reactions to needs.
Neither he nor Darwin explained how the maintenance of integrity in the face of
modifying influences might have originated or evolved. As they are fundamental
emergent properties of life, along with reproduction, any selectionist claim that they
are the product of natural selection can be reduced to the absurdity Natural selection
is the cause of life.
Attrition of the Modern Synthesis

So far the casualty list of the selectionist barrage includes progressive evolution, ortho-
genesis, the organism, mind, and life itself. Although these victims had already fallen
in earlier engagements, the ultras have not stopped trampling upon them. However,
there are other elements of Huxleys original Modern Synthesis that have been ignored
or lost. Epigenetic (or developmental) evolution was once a casualty, but has now
recovered, though suffering from a secondary infection of selectionism.
In the 1940s, after the first flurry of reconstruction, the most important additions to
the Modern Synthesis were the structure, replication, and coding of DNA. These
offered elements of the generative process that had been sadly lacking. But once
molecular biology provided some explanation of how new variants could be produced
as fuel for natural selection, that was all that the Modern Synthesis wanted. It was
unperturbed by the fact that the triumph of reductionismthe discovery of DNA
structureoffered no explanation of differential gene expression. How organisms with
a very similar quota of structural genes came to be so widely diverse was ignored. It
Paradigm Drift 47
had long been known that the chromosome count was of little significance; couch
potatoes have fewer chromosomes than the chips they consume. So it is strange that
the mapping of the human genome in February 2001 trumpeted that one of the
mystifying discoveries is that a human has only 10,000 more genes than a
roundwormas if this presented a brand-new evolutionary puzzle for solution.
Such problems are now being actively pursued by students of developmental
evolution, the self-styled evo-devos (possibly an abbreviation of evo-devo-taries)
who tarried so long before asserting the importance of developmental studies to
evolution and climbing aboard the Modern Synthesis. Their reception was lukewarm,
sometimes hostile, for the others at the captains table were mostly population
geneticists with little feeling for the evolutionary implications of molecular biology.
And traditionally they saw epigenetics as a threat to the ship, by its association with
saltatory evolution.
For Julian Huxley, embryological phenomena were central to evolution, were
heritable, were acted on by natural selection, and were a necessary element of his
synthesis. However, Huxley never integrated his studies of allometry fully into the
Modern Synthesis, and his treatment of differential development was disappoint-
ingly brief, despite the weight he thought it should have. His introduction to the 1962
second edition of Evolution: The Modern Synthesis enthusiastically endorsed
Waddingtons (1957) epigenetic ideas. But he allowed himself to be persuaded by
Rensch (1959) that orthogenesis, part of the original synthesis, should be cast away.
It is also illuminating to read the introduction to the third and last edition (1974),
written by the cream of Oxford evolutionists, hand skimmed by Huxley himself.
Evolutionary embryology, which Huxley had been initially determined to bring into
play, is absent. Physiology? Forget it. In losing such major components, Huxleys
Modern Synthesis regressed to Mayrs version, no longer amalgamating nor unifying,
but providing a bottomless hold-all for any new idea that came along, or old ideas that
became new again. To wield influence, a paradigm does not have to be comprehen-
sive, nor does it have to be based on correct information or sound ideas. It can also
allow empirical applications of false hypotheses. Only with hindsight might they be
seen to have been totally misdirected. What matters most when paradigms are first
established is their psychological or epistemological impact.
Also in 1974, Sren Lvtrup published Epigenetics, a fresh attempt to raise evolution-
ary consciousnessfor those who were awake. Others muttered in their bunks But its
all just genetics!another subset that could be ignored. Optimistic bulletins about
the unsinkability of the Modern Synthesis kept being posted. In the 1978 Evolution
issue of Scientific American it was presented as a perpetual paradigm requiring only
minor adjustments. In The Evolutionary Synthesis: Perspectives on the Unification of
Biology (1980), edited by Ernst Mayr and William Provine, Dudley Shapere sounded
various alarms concerning the loose cannon of reductionism, the rarity of examples of
48 Chapter 1
adaptive mutations from laboratory genetics, and neglect of the discontinuities in the
fossil record.37 But he left embryology and epigenetics out of his muster. Viktor
Hamburger, who was well capable of making amends, merely rationalized the
omissions:
I do not imply a criticism of the originators of the modern synthesis for their neglect of develop-
mental genetics. On the contrary, I would assert that it has always been a legitimate and sound
research strategy to relegate to a black box, at least temporarily, wide areas that although
pertinent would distract from the main thrust. No great discoveries or conceptual advances are
possible without this expediency.38
The first difficulty with this assertion is that something put in a black box ought to be
dealt with as a significant phenomenon whose mechanism is not known, not ignored
as a nuisance. More to the point: what great discoveries or conceptual advances
support such a judgment, and where could a main thrust take a sunken synthesis?
Almost two decades later, even some population biologists and ecologists are
looking beyond the ecological domain of selectionism and realizing the importance of
developmental biology for evolutionary theory. I have already mentioned David Rollo.
Another such ecologist is Wallace Arthur (1997):
We have come to accept a theory of evolution that explains the origin and diversification of
exquisitely-engineered organisms on the basis of the selective destruction of genetic/develop-
mental variants whose initial production has been treated, for the most part, as a black box. . . .
Why has this pronounced lopsidedness of evolutionary theory, with its emphasis on destructive
forces, been allowed to develop?39
Arthur suspects that selectionists, having fought a long war against special creationism
and Lamarckism, are still afraid that if they rest on their laurels these old enemies
might come surging back. The Modern Synthesis has indeed emphasized selection as
a destroyer and an eliminator. But if that redundant role were abandoned, it would
still be as hard to discard natural selection as a materialistic creator, as it was for proto-
evolutionists to discard special creation.
The lopsidedness of the Modern Synthesis was due to the abandonment, or
repulsion of paleontology, the organism, epigenetic saltations, orthogenesis, genetic
assimilation, and the direct effects of the environment. And what do these rejecta
have in common? They participate directly in evolutionary change, and they are minimally
subject to natural selection.
The Rule of Gradualism

One of the perceived flaws of paleontology was that is was soft on saltation.
Saltationism never came close to paradigmatic influence, except when The Mutation
Theory was published by Hugo De Vries at the turn of the twentieth century, and
William Bateson suggested at the same time that Mendelian genetics argued for dis-
Paradigm Drift 49
continuous change. Richard Goldschmidt argued for the saltatory effects of

chromosome mutations and was ridiculed. Later saltationists, such as paleontologists
K. Beurlen and O. H. Schindewolf, were irritations rather than obstacles to the passage
of neo-Darwinism. Despite minor buffeting, gradualism remained a bulwark of neo-
Darwinism and the Modern Synthesis. If a saltatory macromutation is sufficient to
generate a successful new species, natural selection is allowed no part in the transition
except in the spurious role of final arbiter. But if tiny variations are gradually acted
upon by natural selection, to culminate in speciation, then Darwinian honor seems to
be satisfied.
One of the reductions to absurdity of gradualism is hylozoism, also known as
panpsychism.40 According to this principle, if evolution occurs by gradual accumula-
tion and gradual emphasis of pre-existent characteristics, then any feature possessed
at any evolutionary level must have existed in some lesser state at lower levels. Mind,
therefore, must somehow be a property of even inanimate matter. Alfred Russel
Wallace accepted the logic of hylozoism, but since he balked at molecules with mind
he was forced beyond Darwinism:
If a material element, or a combination of a thousand material elements in a molecule are alike

unconscious, it is impossible for us to believe that the mere addition of one, two or a thousand
other material elements to form a more complex molecule could in any way tend to produce a
self-conscious existence. The things are radically distinct. To say that a mind is a product or
function of protoplasm, or its molecular changes, is to use words to which we can attach no clear
conception. You cannot have in the whole what does not exist in any of the parts; and those who
argue thus should put forth a definite conception of matter with clearly enunciated properties,
and show that the necessary result of a certain complex arrangement of the elements or atoms
of that matter will be the production of self-consciousness.41
This demonstrates a distinct contrast between Darwinism and emergentism, because

emergent wholes do have radically distinct properties that do not exist in the parts,
while adaptational aggregations do not. Wallaces own mind, clouded with spiritual-
ism as well as selectionism, could only interpret the emergence of the big brain as a
divine gift, not as an epigenetic saltation. Although hylozoism can easily be reduced
to absurdity, it has attracted strange bedfellows, such as Henri Bergson and Bernhardt
Rensch, whose only other common trait was a deficiency of a sense of the absurd.
Hylozoism also infects some current antichaos studies, with paradoxical conse-
quences. For example, if, despite the contrary stance of emergentism, there were
indeed physical laws that generate complexity and extend to the highest levels of
organization, then evolution would advance without reference to natural selection,
and Lamarckian progressionism would be rationalized.
Gradualism has more recently been the target of a number of hull-breaching
collisions, beginning in 1972 with the punctuated equilibrium of Eldredge and Gould.
They argued that the unevenness of the fossil record was due to periods of relatively
50 Chapter 1
sudden speciation followed by periods of unchanging stasis. Since ontogenic and

population homeostasis resisted change, some kind of genetic revolution was
necessary to overcome it. And they agreed with Mayr (1963) that strong selection
pressures at the boundaries of species distribution were part of the disequilibration.
The result was rapid speciation followed by re-establishment of an even more robust
and hence prolonged genetic homeostasis.
Punctuated equilibrium was not a new idea. Although discontinuities of the fossil
record had always been dismissed as accidents by gradualists, several biologists,
including Darwin, had thought that evolution might have a naturally irregular tempo.
In 1871, St. George Jackson Mivart had compared intermitting periods of
equilibrium in evolution to what would occur in a stable rock pile disturbed by
sufficient force, such as an earthquake. It would rearrange itself into a new configura-
tion that would remain stable for another long phase of inertia.42 The emergence of a
superior organization, though unlikely in a tumbling rock pile, was inherent in
Mivarts view of evolution.
Herbert Spencer constructed a corollary hypothesis, the law of the instability of the
homogeneous or the principle of equilibrium, which held that homogeneous
systems were fundamentally unstable because external forces acted upon them
unevenly. Functional anatomical variations within simple organisms created hetero-
geneous internal forces, and as the biosphere became more complex, so did organisms.
Spencer defined evolution as a change from an indefinite, incoherent homogeneity,
to a definite, coherent heterogeneity; through continuous differentiations and inte-
grations.43 He too thought that progressive stages were followed by static periods of
equilibration, which jibes with the punctuationist and emergentist points of view.
Thus, not only did some Victorian biologists understand the irregular gait of
evolution; they thought there were qualitative differences between rapid and slow
changes, the former saltatory emergences, and the latter adaptations to the external
environment. These were more radical versions of punctuated equilibrium than that
initially advanced by Eldredge and Gould in 1972. However, the latter later allow the
possible involvement of developmental macromutations, as well as catastrophic global
events. The punctuationists use of terms like quirky and herky-jerky echoes
Francis Galtons changes in jerks.44 But although they now embrace epigenetic ideas,
they can barely bring themselves to say saltations, the word for evolutionary leaps
traditionally used by non-Darwinists.
One of the original defenders of gradualism, R. A. Fisher, author of The Genetical
Theory of Natural Selection (1930), argued that evolution by natural selection demanded
gradual change because epigenetic saltations must be maladaptivetoo many
complex systems would be thrown out of order. Embryonic aberrations were not
functional advances that added anything to survival and reproduction; they were
hopeless monsters, doomed at or before birth. However, Fishers real objection to
Paradigm Drift 51
epigenetic saltation as a mechanism of evolution was the same as Darwins: It would

make natural selection redundant.
When the genetic code was discovered, it could be seen how a simple change in a
single nucleic acid base could alter the primary structure of a protein, and possibly
confer selective advantage. At the time, that seemed to be all neo-Darwinism needed.
The importance of chromosomal position effects, gene interaction, and hierarchical
arrays of regulators was ignored. Richard Goldschmidts hopeful monsters were
laughed at as the wild speculations of a man who was not too sure about the reality of
the gene in the first place. Also, Barbara McClintocks research on jumping genes
and her explanations of the evolutionary role of these controlling elements were
resisted by the conservative molecular biologists of the Modern Synthesis as spurious,
and even mystical, for more than 20 years after they first heard of them.45
Neo-Darwinists nevertheless agreed that there were a number of unusually
important novel events in the history of life. Ronald Fisher proposed that recessives
might randomly accumulate in a population until suddenly expressed as dominant
innovations. Ernst Mayr (1960) attempted to accommodate them in the Modern
Synthesis in his essay The emergence of evolutionary novelties. G. Ledyard Stebbins
(1974) identified about 70 of these important emergences in the history of life, and
then commented that their extreme rarity justified focusing attention on the much
more common action of natural selection on simple adaptations. If incongruities
cannot be subsumed, let them be discounted as rare and special cases. Darwin did just
that with Naudins mosaic theory of heredity, which had anticipated Mendelian
genetics.
Luck
Another phenomenon that was rejected early on by the early modernists is the effect
of chance, as opposed to natural selection, on the distribution of alleles in
populations. Fisher had envisioned species as being made up of large populations with
unrestricted gene flow, so that low-probability events would be meaningless. Sewall
Wrights concept of genetic drift, whereby random change could, in small populations,
lead to distributions of alleles affected more by luck than adaptive qualities, was
opposed in the 1930s. But it is now subsumed by the Modern Synthesis, along with
Mayrs founder effect, a principle of some consequence to emergentism.46 Founder effect
occurs if a small population is set up in isolation at the fringes of the parental
population, with a restricted gene pool that has low genetic variability. The founders
might only be a few individuals, or even one gravid female animal or one self-
pollinating plant. Their unusual gene combinations produce unusual organisms, to
the extent of starting a genetic revolution.
Another view of happenstance that came in the wake of DNA sequencing research
was Motoo Kimuras contentious suggestion that many neutral mutations, lacking
52 Chapter 1
detrimental impact, but with no identifiable selective advantage, have accumulated in

all genomes.47 Taking the concept of natural experimentation a step further, Susumo
Ohno thought that repetitive DNA could mutate out of sight of natural selection,
provided that there was an original gene performing its original function.48 This can
also happen at the organ level, as we will see in chapters 2 and 4.
What about the role of chance in large-scale exogenous changes? Cuvier believed the
discontinuities of the fossil record were due to natural catastrophes. Under stable
conditions, all organisms were so perfectly integrated internally, so adapted to their
conditions of life, that any change would be detrimental, and evolution was conse-
quently impossible. Catastrophes caused extinction and change, but not
evolutionorganisms that already existed elsewhere could move into the devastated
environments if they were right for the part. Biologists now believe that Cuvier was
wrong about evolution and right about the natural catastrophes. Yet he came close to
the truth about evolution too. Adaptation reinforces dynamic stability and resists evo-
lutionary change, and extraordinary circumstances are required for it to be overcome.
Being in the right place at the right time, especially in the face of catastrophe, is
another piece of flotsam that has drifted up to the Modern Synthesis. David Raup
(1991) and Stephen Jay Gould (1994) agree that natural catastrophes have been a
major influence on evolution by making new environments available to the lucky
survivors. But as Samuel Butler might have put it, cunning is required as well as luck.49
By cunning he implied physiological and behavioral adaptability, as well as intelli-
gence. Among the lucky survivors of catastrophes, the most cunning organisms would
have the greatest potential to undergo substantial diversification. If this were properly
understood, evolutionists would pay more attention to the emergence and operation
of adaptability, instead of sidelining it as an epiphenomenon of natural selection.
Attempts to define physical rules of complexification barely hint at the evolution of
adaptability in organisms, because the more complicated life gets, the more the
physical rules are superseded. This will become a major theme in the development of
an emergence theory (chapters 2, 8, 9, 10).
Exceptional conditions, such as environmental catastrophe or rare transitions to
new environments, are part of the conventional story. But according to neo-
Darwinism natural destruction and elimination are filters, if not creative forces of
selection. Nothing is said about whats making the coffee. That is, how did qualities
emerge that let the organisms pass through the filters as if they didnt exist, and
survive the consequences?
The idea of release from an ecological straitjacket, combined with the concept that
there is more than luck involved in subsequent biological evolution, could be a
lifeboat for some of the troubled passengers on board the foundering Modern
Synthesis. Indeed, the term ecological release has crept into neo-Darwinism, but it
has done so married to new selection pressures.50 One might also expect neo-
Paradigm Drift 53
catastrophists to question the role of natural selection. If catastrophe provides new

environments, or old ones that have been swept clear of their former occupants, they
will have a clear field. The filters have no significance for the emergent newcomers,
except to prevent competition and predation by those that cannot penetrate them.
Selection theory ignores the causally prior adaptabilities that permit penetration of
new environments, arguing that once the survivors have collected their wits and gone
about their business again they are simply subjected to different and stronger selection
pressures that create adaptive innovations, speed up their spread in populations, and
fill the empty ecological niches. If you find this persuasive, I know of a certain bridge
in Brooklyn that happens to be up for sale.
Darwin himself wrote: When the individuals of any species are scanty, all the
individuals, whatever their quality may be, will generally be allowed to breed, and this
will effectually prevent selection.51 If he had explored all the implications of that
dangerous idea, he might have realized that the very ground of the concept of natural
selection, namely artificial selection by plant and animal breeders, was shaky.
Artificial Selection
Darwin gave artificial selection pride of place in The Origin of Species as the best
analogy for natural selection. But Alfred Russel Wallace said it was the worst analogy:
. . . no inferences as to varieties in a state of nature can be deduced from the observation of those
occurring among domestic animals. The two are so much opposed to each other in every circum-
stance of their existence, that what applies to the one is almost sure not to apply to the other.
Domestic animals are abnormal, irregular, artificial; they are subject to varieties which never
occur and never can occur in a state of nature. . . .52
Populations of domestic animals released from human care reverted to the wild type.
In contrast, natural species would diverge indefinitely, because there would always be
variants that had a better chance to survive under natural conditions. But Wallace
went too far when he said never occur and never can occur in a state of nature. Of
course they can, but when they do they might not fit in with the existing dynamic
stasis. Neither Wallace nor Darwin delved deeply into the more fundamental question:
How could those new variants have originated before the tests of breeder or nature? However,
domestic breeding has a great deal to tell us about what can happen among unusual
congregations in the absence of natural barriers, and how that might be of evolution-
ary significancea logical extension that Wallace failed to make.
Wallaces conception of selection pressure reinforced his opinion that artificial
selection was irrelevant to evolution. Domestic varieties had to be protected from such
natural interference. It also illuminates my argument that they are relevant, in that
they demonstrate what is possible in the absence of such pressure. I wonder if
54 Chapter 1
Wallace was comparing himself, the naturalist toughing it out in the wild, to dilettante
breeders speculating from the comfort of their Victorian armchairs.
Wallaces rejection of the agricultural model did not persuade Darwin. Although the
latter knew that under domestication plants and animals showed greater variability,
including the production of monstrosities, his whole causal hypothesis was founded
on the analogy with artificial selection. What was missing from Darwin and Wallaces
thinking was that neither artificial nor natural selection was creative. What was
selected was generated by unknown mechanisms of biological change. And in both
cases, the selection resulted from the quality of that biological change.
William Bateson, Hugo De Vries, and I. N. Vavilov, who were particularly involved
in the genetics of domestic organisms, were focused on the discontinuity of evolution.
Indeed every biologist is aware of the great range of phenotypic possibilities, such as
homeotic gene expressions in Drosophila that can survive only in protected laboratory
populations. Selectionists get excited about the enormous evolutionary change that
can be effected by the artificial selection of such traits as bristle numbers. To me it
seems more like non-evolutionary change, but in either case it was achieved by
excluding natural selection and genetic dilution.
Many experiments with laboratory populations no longer resort to conscious
selection for particular traits. Instead they imitate nature by modifying the living
conditions for the experimental organisms, i.e., by neo-Darwinist lights, they change
the selection pressures, to see what features are correlated with differential survival or
reproduction. No matter how successful such experiments are, they do not explain the
origin of the correlated features. Moreover, the many predictions based on hypotheti-
cal changes of selection pressures are hit-or-miss, and for the concept to have any
theoretical rigor there would have to be more hits.
The conventional response to such arguments is that the bottom line is always dif-
ferential reproduction, so my distinctions dont matter. But this merely demonstrates
the reverse Looking Glass logic of both Darwinism and the current formal definition
of natural selection. The effect is differential reproduction, but we should be looking
for and then discriminating among causes. Under unnatural circumstances where a
supernatural agentin this case the human experimenter or breederis literally
selecting the organisms to be mated, and consciously removing natural influences, the
result is bound to be differential reproduction. So there is no contradiction to worry
about? Now about that bargain bridge.
In domestic animal breeding programs, sports appear from time to time. These are
emergent novelties, or hopeful monsters that are distinctly unlike their parents. Their
hopes are realized by breeders who deliberately protect them from harmful influences.
They also ensure that these rare emergents reproduce with their own kind, protecting
them from genetic dilution. Inbreeding in minute populations, whether in the wild or
by breeders, brings out quite unusual phenotypes. Under domestication, Darwin
Paradigm Drift 55
remarked, it may be truly said that the whole organisation becomes in some degree
plastic.53 And he knew that some of the products were monstrosities that were bred
from to introduce new strains. In nature, mere monstrosities did not count.
Dmitry Belyaev (1979) found that if Arctic foxes were selected for breeding entirely
on the basis of tameness, hormonal bias brought out dormant genes and produced a
wide range of sports. Close inbreeding was not a factor in these experiments. A
necessary generative condition is the high serotonin levels found in non-aggressive
types, and high estradiol and progesterone that improve fertility and attract males to
females. The pineal gland is particularly plastic under the conditions of domestication,
and its modification has extended the breeding season.54 Consequent behavioral
changes were similar to those found in tame dogs, such as tail erection and wagging,
ear drooping, and licking their human handlers. Piebald sports occurred, some
remarkably like border collies and hence less than ideal for the manufacture of fur
coats.
Belyaevs program excluded foxes with the most competitive or naturally adaptive
traits, such as aggression and fear of humans. And his observations demonstrate how
artificial selection is a much better model for the transformation of radical evolution-
ary experimentshopeful monstersinto successful emergences in the absence of
natural selection and the diluting effects of large populations. He called the process he
discovered destabilizing selection, to contrast it with his mentor Ivan
Schmalhausens stabilizing selection. The latter was part of the process of autono-
mization, whereby environmental influences on the organism were brought under
organismal control. Populations were also stabilized, except at the stressful fringes.
(What biologists imply by the word stress is that physiological and behavioral
responses to environmental extremes are forced to operate at or beyond their limits,
resulting in nervous, hormonal, energetic, and reproductive exhaustion.) The
syndrome of stabilizing selection results in a population which throughout most of its
range has had its stress minimized through co-adaptation of the parts that make up
physiological systems. L. L. Whyte (1965) used a similar concept, which he called
internal selection, to mean an increase in internal organismal efficiency that
decreased the effects of physiological stress. Despite the fact that this aspect of physi-
ological evolution fits quite nicely into the selectionist paradigm, population
biologists have lost sight of Schmalhausens physiological and embryological
inferences. They take stabilizing selection to be no more than regular culling of the
more extreme allelic variations, and subsume it under normalizing selection.
Destabilizing selection is a paradoxical term since in the case of Arctic foxes the
selection is a deliberate human action, and the purpose is not differential reproduc-
tion, but optimal (economical) production of the chosen breeding population. And
indeed natural influences that would usually repress emergents that differed
hormonally and behaviorally are absent. Nor is the stress of an extremely harsh
56 Chapter 1
climate an issue. What Belyaev was observing was an assembly of animals, which
already had certain behavioral and physiological characteristics, into an unnatural
population that would not be able to survive wild conditions. It wasnt so much that
the population was being destabilized as it was that its constituent organisms were
being destabilized, physiologically and behaviorally, because of hormonal disruption
of epigenetic regulation. Variations produced under these circumstances were not
entirely random, nor were they always beneficial to the animals or their breeders.
Despite the unfortunate choice of destabilizing selection as its name, Belyaev had
identified a phenomenon of general evolutionary significance. Although his research
required conscious human interference, Belyaev supposed that the same phenomenon
could occur naturally, especially under stressful conditions.55 What he did not say is
that, although destabilization could occur under natural conditions, normal wild
types and the agents of natural selection would have to be reduced for there to be any
interesting consequences.
Belyaevs prediction that destabilization would occur in the wild under stressful
conditions has been borne out by studies of Siberian hamsters, emperor penguins, and
naked mole rats, whose case histories will be examined in chapter 4. Socialization
produces the same effects in animals that are not under severe stress in the wild,
though environmental influences remain important. For example, the proportions of
different castes of eusocial termites are hormonally manipulated through differential
feeding of the juveniles. Predation stress results in the production of more soldier
termites. And their day-to-day behavior, including nest building, is pheromonally
affected.
Despite the power of analogy between natural and artificial selection, neo-
Darwinists now tend to emphasize the differences between the processes, since they
think, like Wallace, that conditions of artificial selection would rarely occur in nature.
(I regret that having to call a real act of intentional selection artificial, and a
metaphor natural makes the discourse hard to follow.) Like Wallace, they have not
thought it through. If they had looked closer at the significance of artificial selection,
and like Belyaev had sought to find similar natural conditions, they could have
avoided a vexing epistemological problem raised by Karl Popper. In 1959 Popper
argued that selection theory is unsatisfactory because it does not suggest nullifying
experiments, due to the difficulty of controlling differential survival and reproduction.
Quite to the contrary, such experiments have been conducted, for perhaps as long as
12,000 years, with striking results that do indeed refute selection theory. Ever since
humans started breeding plants and animals from marginally useful wild stock,
removal of the agents of natural selection has released a cornucopia of large seeds,
grains, succulent fruits, and numerous domestic animals whose hopeful monstrosity
now appears normal to us. These may have been generated in part by the artificial
selection of broodstock that interacted genetically, epigenetically, physiologically, and
Paradigm Drift 57
behaviorally in novel ways. This was not premeditated, since it resulted from
intentional prevention of genetic dilution, for the purpose of preserving desirable
novelties. None of this was generated by selection; instead it resulted from a series of
natural experiments protected from natural selection by the breeders.
The goal of plant and animal breeders was never to cause progressive evolution in
their fields and flocks, or even to originate new speciesmuch more sensible to
improve a sheep by starting with a sheep and stopping with a better one. However, it
is now possible to genetically engineer new species, and since the mechanisms of
epigenetics are becoming better known, it might be possible to scramble them enough
to produce emergent novelties. Better, perhaps, to confine such experiments to
computer models. But, as I will argue later, the origin of species is little more relevant
to evolution than natural selection. The major focus of emergentism is progressive
improvements of adaptability in the wild that precede speciation. There have been
many phases in the course of evolutionary history where adaptability allowed
organisms the freedom to persist in stressful fringe environments, to survive natural
disasters, and to push on into new territory in the company of similar adventurers.
Whatever causes the progressive improvement of adaptability has the effect of wider
distribution and greater diversification. That would seem to be a major evolutionary
phenomenon, but it is barely considered by the Modern Synthetists. So what do they
make of the causes and effects of evolution?
Causes and Effects
The cause of artificial selection has to do with the intention and action of the breeder,
for example, putting a thoroughbred mare to stud with a race-proven stallion.
Selectionists, however, turn a real intention into a metaphorical one. Causal analysis
of domestic breeding demonstrates that breeders are not responsible for the emergence
of desirable changes in domestic populations, such as flower color, coat patterns, and
novel morphologies. True enough, the action of the breeder to protect the selected
broodstock from the stresses they might find in nature, and to prevent genetic
dilution, hurries the program along. However, what caused those novelties to arise in
the first place should be far more significant for the evolutionist. This brings us back
to a question I asked in my introduction: What cloud of unknowing allowed the
Modern Synthesis to confuse cause and effect in evolution? The miasma began to
develop in the late eighteenth century, with Erasmus Darwins materialism. Trying to
escape the earlier chaos of prime or final causes, such as The Intention of the
Creator, Darwin followed David Humes example and put cause and effect in a
chronological relationship:
CAUSE AND EFFECT may be considered as the progression, or successive motions, of the parts of
the great system of Nature. The state of things at this moment is the effect of the state of things,
58 Chapter 1
which exist in the preceding moment; and the cause of the state of things, which shall exist in
the next moment.56
Neo-Darwinists would admit that differential reproduction is the effect of a variety of

earlier causes including mutation, competition, and sexual selection. Then they would
argue that differential reproduction changes the proportions of alleles in the next
generation of the population, and thus becomes causal. There is certainly a change in
the probabilities of allelic mixing as a consequence, which matters to an organismal
biologist as well as a population biologist. Butand its a big BUTthese new causes
are really the knock-on (or domino) effects of the original causes of generative change.
The deepest logical pitfall here is the confusion of differential reproduction with
simple organismal reproduction. Reproduction, especially if it has a sexual
mechanism, but without the differential qualifier, is itself an important generator of
evolutionary change. It is the point in evolution where the gametes that contain the
organisms evolutionary past are combined in a way that can rearrange the evolution-
ary future. The mechanisms and processes that worked before are innovatively born
again into the organisms of the next generation.
Our neo-Darwinists would probably seize on the previous sentence to say:
Whatever works, or what is adaptive, is what is selected. Therefore theres more of it
in the next generation; energetic inefficiency and inability to beat the competition are
diminished until they reach the point of no returnso, whats your problem? My
response is that whatever works was generated in the first living organisms. The
history of interactions between those organisms and their environment, along with
the experimental nature of reproduction, are causally sufficient to explain evolution.
Improved usefulness or adaptiveness arise as qualities of some of those experimental
evolutionary novelties. Thus, evolutionists should concentrate on the generation of
change and regard differential survival and differential reproduction as epiphenome-
nal to evolution.
When George Romanes described natural selection as the ultimate cause of evolution
(18921897), he was trying to get around the problem of tautological definitions of
natural selection like survival of those that survive. In 1961, Ernst Mayr re-
emphasized the separate categories of proximate causes and ultimate causes in his
analysis of biological causality. Thereafter natural selection was classed as the ultimate
cause of evolution, and the causes of the changes that were selected became
proximate.57 It is an unfortunate semantic accident that proximate hints at triviality,
and ultimate gives a sense of importance, almost as strong as final cause
a Creator, or Aristotles Prime Mover. Mayr has taken a hard line on this, coming
around finally to equating ultimate cause with evolution. In One Long Argument (1991)
he admits to being puzzled by an embryologist who says that the evolutionary signif-
icance of development is not intelligible within neo-Darwinism. And he responds that
studying the mechanisms of proximate causation has never been the job of the
Paradigm Drift 59
evolutionary biologist.58 Thus, at the end of the twentieth century Mayr put himself
on the same platform where E. B. Poulton pontificated at its beginning: So long as
individual variation is present, so long as it is hereditary, it does not signify how it is
produced. . . . So long as it is there it is available, and Natural Selection can make use
of it. Mayr further remarks that in some publications on evolution and development
in the 1990s proximate and ultimate causes are hopelessly mixed-up.59 But they
cannot be quite so mixed up as those publications that confuse cause and effect. In
this book I am going to argue that the proximate causes exhaust the search for evolu-
tionary causation, and that the ultimate cause of natural selection belongs to
non-evolutionary biology.
Ultra-Darwinism
Niles Eldredge thinks that there has been a paradigm shift in the causal theory of
evolution, and that natural selection is once again taken to be the all-sufficient cause.
It should be worth re-examining what he calls the Bible of ultra-Darwinism,
Adaptation and Natural Selection by George Williams (1966). Its author wanted to
remove worrisome accretions such as Waddingtons genetic assimilation, and vague,
or informal concepts of organization and progress. His statement of intent is to purge
biology of what I regard as unnecessary distractions that impede the progress of evo-
lutionary theory and the development of a disciplined science for analyzing
adaptation.60 Ergo, evolutionary theory can progress (by improvements in the
application of selection theory to adaptation) but evolution cannot. He immediately
infers that before the emergence of life there existed molecules in the primordial soup
that could catalyze their own replication:
This is a common chemical property. Even a water molecule can catalyze its own synthesis. Only
rarely would a molecule be formed that would produce chance variations among its offspring,
and have such variations passed on to the next generation, but once such a system arose,
natural selection could operate, adaptations could appear, and the Earth would have a biota.
The acceptance of this account of the origin of life implies an acceptance of the key position
of the concept of adaptation and at least an abstract criterion whereby life can be defined and
recognized. We are dealing with life when we are forced to invoke natural selection to achieve a
complete explanation of an observed system. In this sense the principles of physics and
chemistry are not enough. At least the one additional postulate of natural selection and its
consequence, adaptation, are needed.61
The second paragraph of this quotation would seem more than enough to justify
Eldredges judgment about ultra-Darwinism turning natural selection into a creative
force. But Williams takes it further by echoing Poultons earlier sentiment that the
generative processes of evolutionary change dont matter:
60 Chapter 1
We must take the theory of natural selection and use it in its simplest and most austere form, the
differential survival of alternative alleles, and use it in an uncompromising fashion when a
problem of adaptation arises. . . .
The principle of natural selection is not, as a rule, used by biologists in an adequately
disciplined fashion. It is usually applied to problems like that of long-term morphological
changes, as seen by paleontologists, or to problems of ecotypic specialization (usually climatic),
and cladogenesis. These phenomena make easy demands on a theory of adaptation. Most of the
conclusions on patterns of speciation would be much the same whether based on Lamarckian,
nineteenth-century Darwinian, or modern genetic concepts. . . . Darwins or even Lamarcks
concepts form a perfectly adequate basis for explaining most of the phenomena of systematics.62
The Williams Bible was followed by the New Testaments of Dawkinss The Selfish Gene
(1975), Wilsons Sociobiology (1975), and Maynard Smith and Szathmrys The Major
Transitions in Evolution (1997). Their ultra-Darwinism burns with the same flame of
uncompromising austerity that attracts the moths of evolutionary psychology. If
not a new paradigm, it is certainly a potent ideology with a fine hubris. Its elitist
preemption of criticism is exemplified by Williamss remarks about progress:
I believe that my point of view on the subject of progress and of changes in the mechanism of
adaptation is really the prevailing one in the laboratory and the field and in the technical
literature of biology. It is mainly when biologists become self-consciously philosophical, as they
often do when they address nontechnical audiences, that they begin to stress such concepts as
evolutionary progress. This is unfortunate, because it implies that biology is not being accurately
represented to the public.63
Score one to Williams for the prophetic accuracy of the opening sentence. As to mis-
representing evolutionary biology, the risks of self-consciously philosophical
exposition would seem to apply to ultra-Darwinism as easily as to progress. But it is
progress that has been lost. Richard Dawkins, inspired by Williams, finds progressive
evolution acceptable to the adaptationist where progress implies improvement in
whatever adaptation a specific lineage happens to exemplify. In this sense, evolution
is deeply progressive, and must be so if Darwinian natural selection is to perform the
explanatory role that we require of it, and that it alone can perform. This is quoted
from an undated flyer for Dawkinss video lecture Is Evolution Progressive? It may
be flogging a dead horse to say it again, but since the video was produced with the
cooperation of the Royal Society, London, and the British Institute of Biology it
deserves another whack. Dawkins is essentially agreeing with Williams that progress is
nothing but adaptation, and that it must be so defined to justify the creative role of
natural selection, and its dominance of the evolutionary paradigm.
What of Williamss accusation that biology is being misrepresented? The ultras
proclaim behind the Looking Glass that metaphorical forces are creative; when
challenged, they come out to admit that they are not. And all the time they whisper
that the poor dears cant grasp the complexities of the argument, and any dissent
Paradigm Drift 61
should be stifled because it will give support to those Special Creationists. Reductionist
metaphysics misrepresents evolution as the product of the action of metaphorical
forces on molecular abstractions. Misrepresentation is a chronic condition of ultra-
Darwinism.
Religious Fervor
Paradigms whose popularity is underpinned by polemic, consensus, and belief have a
lot in common with religion. They regularly need new prophets to reinterpret them in
modern language, and they need puritanical zealots to keep them from terminal
moribundity. Re-inventing Darwinism as ultra-Darwinism only demanded an
exorcism of demons, not a qualitative shift. Its roots go all the way back through
molecular reductionism, selfish-gene-ism, the Williams purge, population thinking,
the Poulton manifesto, and the Weismann purification, to the Biblical language of The
Origin of Species that I cited in the opening paragraph of this chapter. Where a principle
is polymorphic in its formal definition, and common usage, it is easy to lose sight of
reality and tempting to reify figures of speech like natural selection and selection
pressure. Religious metaphors such as the cleansing of the temple are common.
Williams uses the light and the way for natural selection in Adaptation and Natural
Selection (1966). This Biblical misquotation is repeated by E. O. Wilson in Consilience:
The Unity of Knowledge (1998). Richard Dawkins concurs that Williamss 1966 book is
the Bible of ultra-Darwinism.64 Dawkins, in turn, has disciples who regard him as their
prophet:
In some ways, Richard Dawkins has been the Martin Luther of biology. Hes the guy who cut
through all the theological mysticism that grew around the true evolutionary church and asked,
Whats the big question? The big questions are the questions you can answer. Any question you
cant is by definition tiny and uninteresting.65
As you may recall, Luther preached salvation by faith alone; reason was the Devils
Whoreso much for reasonable questions, big or small.66 There is no denying the
evangelical success of the ultras. Like the Scottish Covenanters, they stand in the open
with sword in the one hand and the Bible (of Darwinism in this case) in the other. It
is by no means a last stand: their conventicles are drawing curious congregations.
Who then stands in opposition to the ultras? Eldredge occupies the middle ground
along with the naturalists, who are less prone to make assumptions and less theory-
laden. They are, he says, closer to the original ideal of the Modern Synthesis, ever
ready to absorb new ideas about molecular biology, population biology, speciation,
phylogenesis, and ecosystems. We see these entities as simple outcomes of the dual
fact of organismic life: economics and reproduction.67 Without denying his success
at exposing evolutionary extremism, I would de-emphasize Eldredges particular
entities and try to teach him more about the facts of organismic life by addressing
62 Chapter 1
symbiosis, physiology, behavior, environmental causation, epigenetics, and evolution

itself. The catastrophe, constraints, and contingency crowd are not that far from
moderate neo-Darwinism either. Therefore the crisis will not be resolved by any of
these modernist factions.
Now Where?
If modernists cant pull it off, can postmodernists? They argue that the authoritarian
Modern Synthesis should not be replaced with another dictatorial doctrine but should
simply be abandoned in favor of a smorgasbord of relativistic ideas such as structural-
ism, post-Lamarckism, and complexity theory. However, not only does the scalpel of
forensic epistemology antedate postmodernism; it can also be turned on postmod-
ernism. Francis Bacon, who warned against natural theology, saw both the
ultra-Darwinists and postmodernists coming:
They who have presumed to dogmatize on nature, as on some well investigated subject, either
from self-conceit or arrogance, and in the professorial style, have inflicted the greatest injury on
philosophy and learning. For they have tended to stifle and interrupt inquiry exactly in
proportion as they have prevailed in bringing others to their opinion: and their own activity has
not counterbalanced the mischief they have occasioned by corrupting and destroying that of
others.
They again who have entered upon a contrary course, and asserted that nothing whatever can
be known, whether they have fallen into this opinion from their hatred of the ancient sophists,
or from the hesitation of their minds, or from an exuberance of learning, have certainly adduced
reasons for it which are by no means contemptible. They have not, however, derived their
opinion from true sources, and, hurried on by their zeal and some affectation, have certainly
exceeded due moderation.68
I once read this Bacon quotation to a literary postmodernist, and he responded:

Spoken like a true modernist! Im not sure if he meant me or Bacon. However, to
remain whimsical for just another moment, I see myself as an oxymoron: a postmod-
ernist with a mission. It might be tempting to evacuate the grounded flagship of
neo-Darwinism with a zealous fleet of philosophical shrimp boats serving tasty treats,
but I believe they would eventually raft up with the Modern Synthesis and be
subsumed.
Postmodernism gives fair warning that any new theory might settle into another
dynamic stasis resistant to change. Accordingly we need to ask what the minimal
requirements for a different evolutionary synthesis might be, as opposed to a genteel
shift of emphasis, or a flotilla of fresh hors doeuvres. I will offer you a different cuisine,
on a table of emergentism designed to assemble relevant but disparate ideas closely
enough to form some novel associations. It will present evolution as a distinctly
different kind of process than that proposed by Darwin and the neo-Darwinists. A
Paradigm Drift 63
general acceptance of evolution as a saltatory as well as a gradual phenomenon would

be a radical departure, especially if saltations were understood to occur in months
rather than millennia. However, evolution cannot be viewed as an exclusively
saltatory process, since many novelties emerge at critical threshold points along
continuous evolutionary lines.
The causal theory of the Modern Synthesis must be replaced, since its crucial agency,
natural selection, reinforces stasis and obstructs evolution. This is not to be
judgmental about the selection syndrome itself. It is bound to happen when any
resource is limiting, whether or not evolutionary change has occurred. And it is bound
to be re-established soon after evolutionary change gets the opportunity to be
expressed. In this sense, evolution is the author of its own fate, but selection is never
the cause of evolution. Even in lineages where natural selection could be said to
produce directional adaptive change, there may be prior directive, or self-amplifying
molecular mechanisms involved, so that directional selection may be epiphenomenal,
rather than the primary cause of change. As a rule of thumb, the simplest way to deal
with the reverse Looking Glass logic of selectionism is to insert a negative into every
positive claim it makes: Natural selection is [not] the cause of evolution etc.
Selection theory would still apply effectively to quantitative demographics, and to
change in community structure, and to our understanding of how things settle into
energetic stases and then stay that way. These should be recognized as important
aspects of life as a whole, but their quantifications would cease to be regarded as causal
explanations of evolution, and none too soon.
Sren Lvtrup (1975) observed that we should see evolution as an emergent process,
and that history would judge the phase of evolutionism dominated by neo-Darwinism
in the same way as we now see the quaestiones disputatae of the Medieval Scholastics,
such as how many angels could dance on the head of a pin.69 Even if we all shared his
sense of history, the conventional scientific approach to improving evolutionary
theory would still be to establish ones expertise in a particularly relevant field and to
amass hard data that could not be refuted. But research specialization can come down
to counting and sorting the angels on the pin-head. Their dance can be so mesmeriz-
ingly intricate that it is easy to forget that there are larger arenas of evolutionary
causation, and that the significance of a particular one may be quite trivial overall.
With due deference to innovative, specialized researchthe only professional
avenue widely open to academic biologistsa synthesizing overview cannot emerge
from minor local adjustments of facts and figures. Although Darwin had a good
foundation of observation and argument, his historical placement in the development
of biology was a great advantage to getting across a general theory to an eager
audience. Now, we might ask What has become of the scientist more concerned with
the impact that the work of others has on him, than with the impact that his work
64 Chapter 1
has on others?70 My own initial approach is to propose an integrating framework that

has room to accommodate the available evidence and to validate some useful
historical ideas that have been cast away by the Modern Synthesis. This I will
commence in the next chapter.
Meanwhile, since there is not enough room within the Modern Synthesis for radical
change, my first order of the day has been a clean sweep. That many emergences have
identifiable adaptive advantage at their point of origin complicates the argument that
emergentism is a distinctly different approach to evolution. But it does not all come
down to natural selection did it. To perceive a phenomenon as adaptive is not to
explain it. A blinkered search for an adaptive advantage will usually find one that
meets the ecological demands of the moment. But it may be only one aspect of a
greater adaptability that enhances the fundamental integrity of the organism,
allowing it to endure, regardless of ecological conditions, but without conferring iden-
tifiably superior fitness. In Materials for the Study of Variation, With Especial Regard to
Discontinuity in the Origin of Species (1894), William Bateson warned:
No one who has ever tried to realise the complexity of the relations between an organism and its
surroundings, the infinite variety of the consequences which every detail of structure and every
shade of instinct may entail upon the organism, the precision of the correlation between
function and the need for it, and above all the marvelous accuracy with which the presence or
absence of a power of a structure is often compensated among living beingsno one can reflect
upon these things and be hopeful that our quantitative estimates of utility are likely to be correct.
But in the absence of such correct and final estimates of utility, we must never use the utility of
a structure as a point of departure in considering the manner of its origin. . . . It thus happens
that we can only get an indefinite knowledge of Adaptation, which for the purposes of our
problem is not an advance beyond the original knowledge that organisms are all more or less
adapted to their circumstances. No amount of evidence of the same kind will carry us beyond
this point. Hence, though the Study of Adaptation will always remain a fascinating branch of
Natural History, it is not and cannot be a means of directly solving the problem of the origin of
Species.71
It would not be too much of an oversimplification to say that the subsequent history
of the drifting paradigm was largely devoted to attempts to prove such dissent wrong.
It also ignored his suggestion that what was needed was evidence of a new kind, and
more knowledge of the principles of evolution: It is submitted that the Study of
Variation gives us a chance, and perhaps the only one, of arriving at this knowledge.72
Bateson used the word variation in the same sense that I use emergence: as that
process of evolutionary innovation characterized by discontinuity. Although Darwin
believed that variation was virtually continuous, he knew that a proper understanding
of variation would open new fields of evolutionary explanation. However, variation,
as a biological term, has been deprived of that significance by the Modern Synthesis,
coming down to minor changes which are merely fuel for the ecological engine of
Paradigm Drift 65
evolution. And variation has also been corrupted to imply molecular changes so
small as to result in phenotypic continuity. It is thus is no longer available as a
synonym for emergence. But I hardly need to change Batesons exhortation to put it
thus: to get to the essence of evolution we have to explore the generative conditions
and causes of emergence. In them we might find the explanatory power that ultra-
Darwinism claims for natural selection.
From the outset I have taken the calculated risk of outraging conventional wisdom
about the causes of evolution, before making the case for generative emergentism.
Some dissenting evolutionists prefer to avoid controversy by paying lip service to the
notion of the ultimate causal role of selection while giving priority to the proximate
generation of evolutionary novelty. Contra-selectionist and pro-emergentist issues
could be dealt with separately, but it is more satisfactory and less evasive to contrast
them before finally re-integrating them. Nevertheless, if my attempted revision of
natural selection were totally discarded, the need for generative hypotheses to explain
how novelty arises would still be past due.
2
Prologue to Emergence
There ought to be some kind of formal structure that captures the essence of emergence.
Jack Cohen and Ian Stewart, 19941
We will not understand life and living organisms until we understand emergence.
John Holland, 19982
Whenever I reveal my lack of faith in selectionism, I am asked What do you put in

its place? The straightforward answer is emergentism. Yet for anyone who realizes
that selection theory is little more than a theory of demographics, or book-keeping,
the answer is Theres nothing to replace, because there is no causal theory of
evolution.3 Selection theory, if overdependent on metaphorical circumlocution, is
adequate to population biology. However, it fails to account for the generation of evo-
lutionary change. Although this was clearly stated by St. George Jackson Mivart in
1871 in his book The Genesis of Species, the void has never since been filled. Now, more
than a century later, theorists such as Goodwin, Cohen, Stewart, and Holland are
awake to the need for generative principles of emergent evolutionary novelty.
Through the Looking Glass, abstractions and metaphors are creative forces. In
contrast, the emergentist focuses on the organism, looking in at its genetic, develop-
mental, and physiological structure and looking out at its environment and its
responses to it. We dont have to abandon Darwinism altogether; it established the
historical theory in the first place. Moreover, emergences often have significant
demographic consequencesor dominate the ledgersresulting in new ecological
equilibria. These effects must eventually be reintegrated into a larger biological
synthesis, as complementary to the causes of evolutionary change, and a full account
of their history.
While the Modern Synthesis was under construction, evolution, the organism,
mind, and life itself were abandoned. Any attempts to retrieve them are worth a try,
but how shall we go about it? Emergence involves the discontinuous production of
novelty, including greater degrees of complexity. Some introductory remarks about
that are in order.
68 Chapter 2
Complexity
Modern complexity theory is sometimes called anti-chaos theory, since it tries to

make sense of how local complex stabilities can persist in chaotic non-biological
systems. Complexity theory sensu lato, as it pertains to biological systems, has quite a
long tradition within biology, in the writings of E. S. Russell, DArcy Thompson,
Ludwig von Bertalanffy, Joseph Needham, Karl Weiss, Ivan Schmalhausen, C. H.
Waddington, and the early emergentists. But whatever direction complexity theory
has come from, it has not been from Darwinism or selection theory.
Complexity theorists take an interest in biological complexity and its evolution, but
they usually work with computer models rather than real organisms. And although
they often allow a secondary role for natural selection, their quest is not for selection
pressures that produce complexity, but for intrinsic principles that might govern its
autonomous emergence and development. They might, for example, ask: Does the
behavior of gases and water, in forming temporary, semi-stable vortices and
turbulences, inform us of the nature of evolutionary complexification? Does the
behavior of a purely physicochemical system in dynamic equilibrium add to what we
already know about dynamic equilibria in living systems? The short answer is
Probably not. Any complex system can be compared to any other complex system,
and equations can be derived, without offering any idea of how a new emergent level
arises from the lower generative level. Biological innovations are not bound by the
laws of physics in the same way that purely physical systems are. In fact, interpreta-
tions of complex physicochemical systems have probably been informed more by the
application of organismal ideas than the other way round. All the same, explorations
of non-equilibrium thermodynamics and chaotic attractors are fascinating and
stimulating.4 If their models demystify the complexification of organisms to some
extent, good and well.
Most biological complexity theoreticians seek to avoid controversy by accommodat-
ing natural selection before moving on to the main business. For example, Michael
Conrad (1990) writes that evolutionary organization results from self-complication
and asks Why does evolution work? He writes: The reason is not to be found solely
in the magic optimizing power of variation and selection. It is as much due to the
organizational structure that undergoes the variation. Evolution works because this
organization is amenable to evolution, and because this amenability itself increases in
the course of evolution.5 Conrad equates organizational improvements with adapt-
ability, which has the additional qualities of reliability and stability. So be it. They
are self-sufficient and improvable properties of the kind that have characterized life
since it first emerged, without any necessity for the redundant judgment of natural
selection. For Conrad, however, progressive organization can only persist by
hitchhiking along with the advantageous traits whose appearance it facilitates.6
Prologue to Emergence 69
Although he is on the right road, a more holistic interpretation would see organismal
progressive organization not as the hitchhiker but as the whole vehicle and its
contents. It not only carries traits that are immediately advantageous, but has multi-
functional features that will be advantageous under different circumstances. They are
not picked up one at a time along the way.
Furthermore, organizational progress might have no adaptational features in the
short term. Its quality is its integrity, which is sustained through greater adaptability.
The organism can now go on doing the same thing when conditions change, and do
different things when conditions stay the same. But such self-sufficient improvements
may not amount to a competitive phenotypic fitness in a stable ecosystem.
Furthermore, specialization may lead to regression of former adaptability. For
example, most fish that live permanently in fresh water have lost their ancestors
adaptability to deal with salt water as well.
In a similar vein, Stuart Kauffmans book Origins of Order: Self-Organization and
Selection in Evolution (1993) begins as follows:
We must understand how such self-ordered properties permit, enable and limit the efficacy of
natural selection. We must see organisms in a new light, as the balance found, the collaboration
achieved, when natural selection acts to further mold order which pre-exists. In short we must
integrate the fact that selection is not the sole source of order in organisms.7
My own conviction is that natural selection is neither the sole source, nor any source
of order at all except demographic equilibrium. Any increase in order improves
organismal integrity, and so will persist if its energetic requirements are met. Thus, it
will be perceived to have selective advantage. But its energetic requirements may not
be met if there is strong competition from the pre-existing organisms in a state of
ecological dynamic stability. Persistence may be better realized in fringe environments
where competition is low. Once established, the new emergents should hypothetically
shake down into an even more resistant equilibrium. However, some lineages have
been able to periodically overcome that resistance.
The Reduction of Complexity

In the context of complexity, it is necessary to talk about reductionism, a word that
is often used very loosely because everybody knows what is meant. If that were
really so, there ought to be a clear distinction between reduction and reductionism,
but biologists tend to lump them together. For example, the triumph of reduction-
ism, as the discovery of DNA structure is often called, should be the triumph of
reduction.
Reduction is an epistemological tool for understanding complex structures by
analyzing their components. Its successful application is demonstrated by Watson and
Cricks 1953 discovery of DNAs structure, which suggested the basis of reproduction
70 Chapter 2
and the genetic code. The problems of reproduction and heredity, originally asked at
the organismal level, were reduced to the molecular level, and came to fruition when
returned to the organism. Reduction is a neutral epistemological method, whose value
is to be measured in how usefully it can be referred back to the original problem.
However, reduction with -ism tacked on represents a biased worldview. In
Consilience (1998), E. O. Wilson remarks:
Beyond the mere smashing of aggregates into smaller pieces lies a deeper agenda that also takes
the name of reductionism: to fold the laws and principles of each level of organization into those
at more general, hence more fundamental levels. Its strong form is total consilience, which holds that
nature is organized by simple universal laws of physics to which all other laws and principles can
eventually be reduced. This transcendental world view is the light and way for many scientific
materialists (I admit to being among them), but it could be wrong. At the least, it is surely an
oversimplification. At each level of organization, especially at the living cell and above,
phenomena exist that require new laws and principles, which still cannot be predicted from
those at more general levels. Perhaps some of them will remain forever beyond our grasp. Perhaps
prediction of the most complex systems from more general levels is impossible.8 [emphasis
added]
Wilson values reductive methodology and understands the obstacles to predicting

complex systems from their simpler constituents. But despite his reservations, the
sentence that I have italicized infers that to understand complexity, final reduction to
physical laws is necessary. Apotheosis of reductionism to the light and the way is
transcendental, but not original.9 In the past it was holism that was committed to the
flames for its transcendental qualities. Wilson rescues holism as consilience by
synthesis, but subordinates it to the reductionism of total consilience. It is an easy
step from Wilsons relatively balanced view to a doctrinaire reductionism that infers
that the only way and light is through upward causation driven by physical laws. Its
natural disciple is the molecular biologist.
Some students of complexity are critical of reductionism, having a greater apprecia-
tion of emergent properties of organismal levels that cannot be predicted from a
knowledge of molecules. J. H. Woodger (1929) warned against intolerant abstraction
that abandoned the whole once it had been reduced.10 Along the same lines, William
Wimsatt (1997) remarks that the difference between a biophysicist and a theoretical
biologist is that the first is only interested in the invariate aggregative properties of
organisms once they have been put through a blender and fractionated by centrifuga-
tion. He believes (regrettably, not always a valid proposition) that the biological
theoretician is interested in how those properties interacted in the organism to make
it a whole greater than the sum of its parts before it went through the blender.
Wimsatt calls the nothing-but atomism that he understandably dislikes vulgar
reductionism.
Systems Reduction
Evolutionary complexification has parallels with the developmental complexification
in the individual organism as it grows from zygote to adult. In How the Leopard
Changed Its Spots (1994), Brian Goodwin writes:
The sciences of complexity lead to the construction of a dynamic theory of organisms as the
primary source of the emergent properties of life that have been revealed in evolution. These
properties are generated during the process known as morphogenesis, the development of the
complex form of the adult organism from simple beginnings such as an egg or a bud. During
morphogenesis, emergent order is generated by distinctive types of dynamic process in which
genes play a significant but limited role. Morphogenesis is the source of emergent evolutionary
properties, and it is the absence of a theory of organisms that includes this basic generative
process that has resulted in both the disappearance of organisms from Darwinism and the failure
to account for the origin of the emergent characteristics that identify species.11
I will assess this salient in chapter 10. But Goodwin and several others who follow
similar themes often use expressions such as emergent order, emergent properties,
and emergent evolution without distinguishing, defining, or even indexing them,
as if they are epiphenomena of universal rules or algorithms of complexity. Instead of
reducing complexities to the fundamentals of physics and chemistry, they apply
systems reduction. This means that they examine simpler organized systems that appear
to have the same qualities as the complex ones. These are easier to analyze, while suf-
ficiently ordered to help make sense of the really complicated ones. This is much more
useful than simplistic molecular reduction.12 But even if we knew of an algorithm that
dictated how a new level of complexity is obtained at a given emergent level, it would
not necessarily apply to, and so predict or explain the generation and nature of the
next emergent level up.
The power of systems reduction also attracts Jack Cohen and Ian Stewart, authors of
The Collapse of Chaos (1994). They keep vulgar reductionism strictly at the end of a
barge pole while they quant among emergent phenomena. Nevertheless, for them,
natural selection is the evolutionary metarule that causes complexification.
Flaunting the redundancy that lies in survival of the fittest, they declare: The
complexity of a living organism is the result of an evolutionary game played over huge
periods of time according to a rule so simple that it is really just a logical tautology.
Winners win.13 Then they remark, quite unselfconsciously, If a theory is so flexible
that it can explain anything whatsoever, its probably nonsense!14 If this is heavy
irony, I have to admit to being caught out.
One of Cohen and Stewarts models of an emergence anticipates what is to come in
this book, and at the same time illustrates their paradoxical view of natural selection
as the cause of evolution. An imaginary creature experiments with the accumulation
of hydrogen and takes to the air as a balloonist. To begin withno competition up
therethey would thrive, just as the winged creatures did along our evolutionary
72 Chapter 2
track.15 Subsequently they imagine an environment where the emergent forms fill up
the available space. Now, the scene will be set for genuine evolution, by competition,
selection, and reproduction of those . . . that survive.16 Plus a changeby this
Looking Glass logic the generative process, emergence, and the thriving of its creature
in a space free of natural selection is not genuine evolution. (I hope this is more
heavy irony.) In the real world, by way of contrast, evolution tries through natural
experiment, and succeeds in the absence of natural selection that enforces stasis.
Surveying and explaining the natural experimental methods of evolution, and
discovering how the opportunities for success present themselves, are the tasks of
emergentism.
Origins of Emergentism
The roots of emergentism lie in the classical Greeks concept of order coming out of
chaos, and their debate over whether it happened by chance or necessity. Was it the
occasional effect of unpredictable combinations of simple forms, or the result of
design in nature? Aristotle made much of the nature of wholes, especially those that
were greater than the sums of their parts. Emergent properties are what make them so.
The great second-century anatomist and physiologist Galen also distinguished
between the resultant and emergent qualities of wholes.17 The question of how chance
or necessity might be involved in the production of more complex wholes remains
open, even among materialistic evolutionists. Emergent change could be purely a rare
and random accident that increases complexity of structure and function. Or it could
be an expression of the operation of natural physical and biological tendencies toward
complexity. The eventual answer may be found to combine both.
Hegel had an emergentistic, metaphysical vision of the revolutionary progression of
life from non-living to living to conscious and then to spiritual. Also, Kant perceived
that in the development of an organism simple parts interact to produce a progres-
sively complex series of emergences of functional forms, in contrast to a machine that
is an assemblage of pre-manufactured parts. Writing in the Enlightenment era, Kant
was influenced by the thoughts of Buffon and his compatriots on natural adaptation
and the effect of the environment, but he did not apply his analysis of emergent
development to biological evolution. And he came to believe that living phenomena
were irreducible because they were purposeful, rather than that they naturally evolved
through discontinuous stages of emergent complexity.
Kants distinction between the assembly of mechanical components and certain
kinds of complex systems carried over into the nineteenth century, when John Stuart
Mill (1843) pointed out that chemical compounds have novel features that cannot be
predicted from a knowledge of their elements. George Henry Lewes (18741875) noted
that these emergent qualities are distinguishable from additive resultants. And
emergent qualities are especially characteristic of organisms. When biological

elements are compounded, novel features are generated. Only the natural combining
qualities of the components need be considered. Although this should have made any
additional vital force redundant, the vitalists loved it, and transcendental
emergentism became the bedfellow of Henri Bergsons doctrine of the lan vital. This
vital spark sprang from a universal primordial consciousness, to energize evolution.
Even so, the transcendentalists tried for a degree of objectivity. Henry Drummond,
though an evangelical member of the Free Church of Scotland, eschewed creationistic
vital forces in The Descent of Man (1894):
When we pass from the inorganic to the organic we come upon a new set of lawsbut the reason
why the lower set do not seem to operate in the higher sphere is not that they are annihilated,
but that they are over-ruled.18
Drummond also realized that greater complexity brought greater adaptability.

The self-styled realist Samuel Alexander regarded godliness as a primordial property
of matter from which deity would finally emerge, life and mind being the intervening
stages. Yet in Space, Time and Deity (1920) he came down to earth sufficiently to
establish that emergences had properties that overruled the demands of the lower
levels of organization:
The higher quality emerges from the lower level of existence and has its roots therein, but it
emerges therefrom and it does not belong to that lower level, but constitutes its possessor a new
order of existent with its special laws of behaviour.19
Compare Drummond and Alexander with John Holland (1998):
If we turn reductionism on its head we add levels. More carefully, we add new laws that satisfy
the constraints imposed by laws already in place. Moreover these new laws apply to complex
phenomena that are consequences of the original laws; they are at a new level.20
C. L. Morgan and Emergent Evolution

The chief progenitor of evolutionary emergentism, Conwy Lloyd Morgan, was a
zoologist, comparative psychologist, and student of T. H. Huxley. His first major con-
tribution to theoretical biology, in 1896, was his independent formulation of genetic
assimilation, as a version of it was later called by C. H. Waddington. J. M. Baldwin
and H. F. Osborn coincidentally wrote about the phenomenon in the same year.
Morgan began to lose faith in Darwinian evolution by natural selection, shifted
toward emergentism, and he had a powerful influence on Samuel Alexander.
While Morgans Emergent Evolution (1923) established the central idea, it was
deficient in examples and explanations. The Gifford Lectures, on which the book was
based, demanded a natural theological context, and he struggled with general
metaphysics and the role of the Divine. While his training, research and historical
74 Chapter 2
placement uniquely qualified him to provide a materialistic biological interpretation,

he never got round to it. And by declining to commit to sudden, large-scale,
qualitative evolutionary change, he was actually less adventurous than Alexander.
Morgan concluded that an emergence might have the appearance of saltation but was
best regarded as a qualitative change of direction or critical turning point.21 Thus,
continuity was preserved, even where it looked as if a novelty had leapt into existence.
This is a legitimate but not exclusive example of emergent phenomena to which I will
refer, in deference to Morgan, as critical-point emergence. This may strike a familiar
chord with those aware of Per Baks principle of self-organizing criticality, which posits
that gradual cumulative changes may reach stages where novel characters are
revealed.22 These critical-point emergences are equivalent to the threshold effects that
are important in developmental evolution. Moreover, some may be predictable if they
follow a linear progression. Therefore, unpredictability is not a sine qua non of
emergence, as the early transcendental emergentists believed.
However, despite Morgan, some emergences are both unpredictable, and saltatory.
These are the ones that grab the attention of emergentists, and so some philosophers
of science call them strong emergences. They call critical-point, threshold events
weak emergences. They are not terms that I will use, since they invite invidious
comparison.
As to causation, Morgan had a more complete interpretation. The causes of
emergence could be either immanent (= intrinsic, arising autonomously from the
dynamic structure of the organism) or transeunt (= extrinsic, having an external
cause). The latter would obviously depend on environmental conditions, but Morgan
did not delve further into such contingencies.
I am now attempting what I think Morgan could and should have done 80 years
ago.
The original conceptions of emergent evolution, while never totally denounced as
heresy, had three strikes against them. First, there was the proposal that emergences
were caused by vital inherent tendencies. Second, it made much of spiritual emergent
levels at a time when transcendental theories were being eclipsed by materialism.
Third, there was intense competition from the second wave of neo-Darwinism, based
on gradualistic theoretical population genetics.
Christopher Caudwell wrote a clear, simple, and non-vitalistic view of emergent
evolution in 1935. But it was not published until 1986. This parallels the case of
Friedrich Engelss The Dialectics of Nature, written in the late nineteenth century but
not published until 1926. Both of these Marxist authors had found an emergentism
that they could reconcile with materialism. Caudwell, who died during the Spanish
Civil War in 1938, saw evolution as a series of steps:
. . . at each step the environment has become differentthere are different laws, different
problems, different obstacles at each step even though any series of steps despite its differences
has certain general problems, laws and obstacles in common. Each new step in evolution is itself
a new quality, and this involves a newness which affects both termsorganism and
environment.23
Recent Approaches to Emergence
In Evolutionary Theory: The Unfinished Synthesis (1985), I discussed the early history of
emergentism and holistic biology, and suggested that the concept of emergence could
be the foundation of a novel evolutionary synthesis. Shortly before that, in 1983, the
neurophysiologist Roger Sperry had written about the evolution of mind as an
emergence, a point of view that had persisted among some psychologists and anthro-
pologists, during the half-century eclipse of biological emergentism. The emergence of
cognition, or mind, still enjoys a large independent literature. Sperry described his
own recognition of emergence almost as an epiphany:
My long-trusted materialist logic was first shaken in the spring of 1964 in preparing a nontech-
nical lecture on brain evolution in which I was extending the concept of emergent control of
higher over lower forces in nested hierarchies to include the mind-brain relation. I found myself
concluding with the then awkward notion that emergent mental powers must logically exert
downward causal control over electrophysiological events in brain activity. Mental forces were
inferred to be equally or more potent in brain dynamics than are the forces operating at the
cellular, molecular and atomic levels.24
This illustrates what Sperry called the interactionist relationship between

emergence, hierarchical structure, and causation. It is not difficult to understand his
point. When we think about something we can conjure up sensory memories, and
with a little practice learn to stimulate adrenaline release or even alter our heart rates.
Later commentators on emergent evolution have suggested a variety of ways to
assess its causes, properties and epistemological value, which I deal with in chapter 8.
For the time being, I will simply add that several biological authors besides Jack
Cohen, Ian Stewart, and John Holland (quoted at the beginning of this chapter) are
aware of the importance of emergence and the need for its formal treatment. Susan
Oyama (2000) surveys the challenge of an unknown terrain thus:
In what ways does the emerging organism evoke, seek, produce, or reliably have supplied for it
the very stimuli and conditions it requires for further development? How does it interact with
them? What are the ways this entrainment can be derailed? What are the possibilities for com-
pensation when such derailment occurs? Surely these possibilities are themselves dependent on
conditions that may vary. How do some early variations become amplified, while others are
damped? Propensities, potentials, stability, and lability are characteristics of systems in progress,
and it is up to us, using the more productive lines of inquiry from behavior genetics, physiology,
ethology, and related disciplines to analyze developmental systems of interest to discover how
various inherited interactants are related.
76 Chapter 2
When an environmental variable is found to be confounded with genotype, we have located

an aspect of developmental order, an association that may well order future development. These
are the associations we must investigate in order to understand how each structured developmen-
tal state arises, for it is this state that will be an important determinant of subsequent
interactions. Such confoundings, then, are not dross to be eliminated by better experimental or
statistical control. They may be the very gold we are seeking, and the point of control is to
illuminate the ways mutual selectivity works.25
To give her due priority, I note that Oyama was already discussing these matters in her
1985 first edition of The Ontogeny of Information: Developmental Systems and Evolution.
Brian Goodwin has also staked a claim in this venture, and Stuart Kauffman writes that
a theory of emergence is the proper goal of complexity studies.26 John Holland, a
computer scientist and a psychologist, approaches a mathematical theory in Emergence:
From Chaos to Order (1998) and concludes that the next steps to be taken in the
development of a theory of emergence will have to proceed along the following route:
Usually the persistent patterns that arise in these generated [emergent] systems are not easily
anticipated on direct inspection of the generators and constraints. The most lucid examples of
emergence arise when these persistent patterns obey macrolaws that do not make direct reference
to the underlying generators and constraints. [Examination of a] minimum of three levels will be
necessary to arrive at a representative body of theorems relevant to emergence: mechanism >
agent > aggregate. Formally we might only consider two levels, treating all higher levels as
recursions of these basic relations. With no very sound argument to back me, I think the three-
level study will be more revealing and more productive as a first step.27
It is important that Holland says body of theorems rather than a single formula.
Even at a third level there is neither a universal rule nor equation of emergent
evolution that applies to the whole. For two that are highly distinct, compare the
emergent complexification of eukaryotes by symbiosis and the autonomous
emergence of mind as a novel quality of the hominid brain. Aggregate is an
unfortunate term, since it is commonly used for resultant wholes in contrast with
emergent wholes that are greater than the sum of their parts, and I am sure Holland
does not intend otherwise. There is a profusion of mechanisms and novel macrolaws
(= emergent rules of organization) in all organismal hierarchies, whether they be
molecules, unicells, symbiotic complexes, multicellular organisms, populations,
societies, demes, communities, or ecosystems. So they need to be sorted out and
clarified.
In the following five chapters, I combine facts and concepts pertaining to emergent
biological processes before proceeding to theoretical generalizations in chapters 811.
Instead of dealing with each of the hierarchical levels that I have just mentioned,
starting with the simplest and ending with the most complex, I deal with causal arenas
that match traditional divisions of biology. In each of these, hierarchical structure can
be discerned.
All biologists agree that organisms are hierarchically constructed, and that such a
perception is epistemologically useful. But I must caution that some reductionists
reject the implication that hierarchical structures contain irreducible emergent
properties. As Jaegwon Kim (1999) presents their argument in Making sense of
emergence, emergent properties are only meaningful if they are mechanistically
causal, and, if they are, their hierarchical levels must be reducible to physics. Hence,
they conclude that any talk of an emergence doctrine is empty. The hollowness of
such inferences is exposed by Peter Corning in his 1998 essay The synergism
hypothesis:
The term emergence is especially popular among die-hard reductionists, because it implies that
wholes are merely epiphenomenal effects of laws and causal processes that can be fully
illuminated at lower levels.28
The problem of reductionist-emergentists is that, in attempting to model complex

physical systems, they assume that all emergent phenomena, whether empty or
fruitful, can be explained from the bottom up. However, they will not succeed in this
goal, because the operation of new constraints and interactions at new emergent levels
is refractory. In fact they have given themselves an excuse for not trying! My thesis is
that emergent properties do exist, and that they have a mechanistic causation that
operates up, down, and across hierarchical levels. They might be reduced to physical
principles by anyone with the competence to deal with all of the hierarchical levels
involved, and the urge to do so. But they cannot be predicted from the bare laws of
physics without smuggling the properties of higher emergent levels down to the foun-
dational laws. For example, the operation of a nerve might be reduced to the action
of electrons or ions. But to go from electricity to the nerve requires passage through
several levels of organismal complexity, none of whose emergent properties can be
predicted or even projected from physics. My own pragmatic preference is to go
straight to the generation of biological change, taking hierarchical structure into
account as I proceed. Indeed, my next chapter on symbiosis and association does go
from simple subcellular structures to complex societies. The chapter on physiology
shows how functional anatomy has gone from a simple state of conformity with
environment to an independent, organized state of homeostasis, through evolution
within existing hierarchical levels as well as by the addition of new ones.
Developmental biology illustrates how hierarchical structure and its emergent levels
are rebuilt from simple origins in every generation. This can then be related to evolu-
tionary history. For each causal arena I intend to outline what there is, how it got that
way, and how it can be explained by evolutionists.
Without a few more conceptual guidelines my exposition might seem aimless or
dislocated. Therefore, imagine we are going on a field trip, and our first stop is the
emergence circus. As we set out, I offer the new explorer the following program of
78 Chapter 2
emergent evolutionary performances, and a field trip checklist will come at the end of
the chapter.
Outline of an Emergence Theory
When I discussed the flaws of the Modern Synthesis, I argued that any alternative had
to include a better generative hypothesis than the action of natural selection on
genetic variation by mutation. If the necessary set of principles can be identified, we
will have advanced toward a theory of emergent evolution. Emergence is commonly
associated with the discontinuous, unpredictable generation of brand-new biological
features, with increased complexity and self-organization. But there are varying
degrees of discontinuity and novelty. Although non-biological phenomena can
emerge in time with novel qualities, my version of emergentism largely deals with all
processes of evolutionary change, together with their generative conditions,
mechanisms, and emergent properties. It combines the emergentism of the 1920s with
those of later commentators, as well as my own opinions. The numerical success of
new emergents in populations depends on unpredictable but affective contingencies,
or accidents if you will. These also have to be taken into account, and this aspect of
emergentism finally interfaces with the demographic theory of selection. If most of
the history of life and the ordinary activities of organisms are non-evolutionary, or
merely trivial in their evolutionary content, it would be constructive finally to clarify
what how evolution and equilibrium have complemented each other in the history of
life, and that will be considered in chapter 11. For the moment I will begin to correct
the reverse Looking Glass logic of the Modern Synthesis by negating its axioms:
Evolution is [not] caused by natural selection.
Cumulative adaptation is [not] progressive evolution.
Evolution is [not] exclusively gradual.
Evolution is [not] slow.
The origin of species (i.e. speciation) is [not] the pivotal process of evolution.
Evolution is [not] change in the distribution of alleles or genotypes in populations.
Now we need something to put in their placean equivalent series of positive

aphorisms to anticipate my thesis:
Evolution happens through natural experimentation. While it involves reproduc-

tion and differentiation, it is distinct from differential reproduction.
Progressive evolution is a cumulative, hierarchically ordered series of emergences

with qualitative novelties of morphogenesis, physiology, behavior, and association.
Emergences produce wholes that are greater than the sum of their parts.
Emergences are sudden on the biological time scale, happening at the speed of
biochemical, physiological, developmental, and behavioral reactions.
They may lead to adaptational specialization, which limits evolutionary options, or

to greater organismal adaptability, which proffers greater freedom of choice for
individuals.
Emergence may be directly caused by environmental change, though ultimately

genetically based.
The actions of individuals are crucial in shaping the evolution of their descendants.
Arising from the previous two points, many emergent conditions that are now
regarded as genetically heritable are preceded by non-heritable events (behavioral
actions, environmental effects and developmental, physiological and behavioral
responses.)
The uniqueness of the phenotype, and hence the dynamics of the underlying
genome as a whole, is more relevant to evolution than individual genes and
proportions of alleles in populations.
Emergences may be all-or-none saltations, or critical-point (threshold) innovations,

both complexifying and regressive, that punctuate allometric trends or orthogenetic
drives. (Regressive may seem contradictory; but sometimes the loss of an inhibiting
character opens up new possibilities for experiment.)
Spurts of emergent evolution are followed by diversifying evolution (adaptive

radiation), which peters out into long periods of stasis reinforced by the agencies of
natural selection. These equilibrium phases temporally dominate the history of life.
Reproductive isolation preserves emergent novelty. Speciation may simply be a by-

product. The aspect of reproduction also distinguishes biological emergence from
physicochemical emergence.
80 Chapter 2
To supplement the above bare-bones synopsis, there follow some capsule commen-
taries on principles or phenomena relevant to the modes of emergent evolution.
Modes of Emergent Evolution

We have seen that evolution is defined by selectionists as changes in the distribution
of alleles in populations. More enlightened modern synthetists recognize the
importance of phenotypes, which equate to whole organisms. And some define
evolution as transgenerational changes in organisms, i.e., they are only evolutionary
if they are heritable. But what does evolution mean to an emergence theorist? I have
already adumbrated two kinds of evolution: progressive and adaptational.
Progressive evolution is equivalent to increase in complexity, which is discussed
above. The most important point is that progressive evolution brings increased adapt-
ability, which allows organisms to persist in an ever wider variety of environments.
This kind of evolution is most likely to be saltatory and to result in emergent
properties that will govern future evolutionary events. The non-biologist is very much
interested in examples of progressive evolution, such as the emergence of complex
organisms from bacterial ancestors, and the emergence of humans from the lower
primates.
Adaptational evolution occurs in relation to specialized habits and distinct habitats.
Its most radical forms are divergences that result from emergent improvements in
adaptability, combined with some kind of release from the constraints of hypostatic
natural selection. It produces specialized body forms and habits such as are found in
most classes of organism, and is therefore the most visible to the observer, and most
identifiable to non-biologists as evolutionary adaptation.
Nearly all aspects of progressive and adaptational evolution are heritable, and
require a DNA component as part of the system. Emergence theory will engage the
question of when DNA enters into the evolutionary process. It will also subsume
hereditary factors which are not DNA-based. Moreover, environmental factors that
consistently and persistently influence the operation of hereditary mechanisms must
also be accounted for.
The modes of emergent evolution involve natural experiments that result in a
combination of discontinuous, saltatory evolutionary emergences, and self-amplifying
drives that reach critical-point emergencesin contrast to slow, gradual evolution
through the accumulative action of natural selection on random gene mutations.
Emergentism primarily attends to the progressive evolution of coordinated
complexity. Diversifying evolution is not to be seen as a simple process of adaptive
radiation, but as the result of a combination of causes and effects including epigenetic
and physiological emergence, and orthoevolutionary mechanisms other than
directional selection, as well as adaptation in the traditional sense. Natural selection is
taken to be a real syndrome of intermediate causes and effects arising from emergent
qualities. It leads to adaptation and ends in rigid specialization. And, in doing so, it
obstructs progressive evolution by establishing dynamic stases affecting development,
physiology, associations, and ecosystems. At the same time it reinforces the
foundations, especially physiological coordinative conditions, from which new
emergences can spring.
When new emergent properties appear the consequences that are most apparent in
the fossil record are diversifying evolution, but this may not occur until the restraints
of natural selection are removed. Those emergent innovations that are able to escape
those restraints are not bound by old rulesan emergent homeotherm need not slow
down when the ambient temperature drops. The primary causes of emergent
evolution are epigenetic (embryological), symbiotic-associative, physiological-
behavioral. And the environment affects all of these primary causes, through direct
physicochemical changes, genetic assimilation, and the disequilibration of ecological
stasis. Catastrophic change not only weakens or removes the obstacle of natural
selection; it might also physically initiate new epigenetic evolutionary experiments.
For example, heat shock from sudden climatic change or catastrophic volcanic and
bolide impacts might increase mutability, through the epigenetic influence of stress
proteins.
The major evolutionary emergent properties of animals amount to increased adapt-
ability in individuals. Through emergence to higher levels of physiological regulation,
a more sophisticated homeostasis confers greater freedom of choice and action. The
freedom of greater adaptability has historically led to an increased potential for diver-
sification (adaptive radiation) of the novel, emergent types. Eventually the emergence
of mind allows analysis of options before commitment to action. Charbel El-Hani and
Sami Pihlstrm note in their 2002 essay Emergence theories and pragmatic realism
that the early pragmatist tradition is characterized by the frequent use (by philoso-
phers like James, Dewey, Mead, Charles Hartshorne, Sidney Hook, and Ernest Nagel,
among others) of notions such as creativity, freedom, evolution and novelty, which
quite naturally find a place in emergentism.29 I enthusiastically combine such
optimistic notions throughout this book, although I find the biological processes and
consequences of emergences more interesting than their ontological analysis. But how
can we assess the potential of any organism to undergo emergent evolution?
Modularity
Progressive evolution of complexity is possible because of biological modularity,
which involves a multiplicity of varied organic holons, or modules, such as exons,
genes, multigene modules, protein domains, biochemical pathways, cells, and organs.
These units can be shuffled, replicated, transposed, and mutated. Therefore,
redundant copies are necessary components of evolutionary experiments. More
important for the proper development and functioning of the organism are their
82 Chapter 2
integration, interaction, and self-organization, which involve a multiplicity of

modifier genes, gene-regulating proteins, hormones, receptor molecules, sensory
organs, neurons and their dendritic connections, and a circulatory system. Also
implicit is a hierarchical ordering that allows them to be regulated efficiently en masse
while leaving them some freedom to operate and to change independently. This is
important both for the evolutionary potential of the organism and its adaptability as
an individual. It can be generalized that, if a self-reproducing entity has a modular
structure, it can become more complex, it can remain the same, or it can regress. In
evolutionary history there are striking examples of all those options.
Adaptability
Progress, or complexification, can be largely equated with increase in the adaptability
of organisms, a feature that maintains organismal integrity, one of the emergent
qualities of life itself. In 1896, James Baldwin called it a blanket utility, because right
from the beginning it can survive a range of challenging circumstances. As Darwin
surmised, improvements in the ability to persist in being are self-sufficient, in
contrast with qualities that are naturally selected according to environmental
conditions. Since the full potential of adaptability is out of sight of natural selection,
its fitness rating is only as high as that of its operating features under limited circum-
stances. Specific elements of adaptability may become specialized if internal and
external conditions remain constant, with the result that adaptability often regresses.
Adaptations on the other hand are genetically fixed, inflexible, and appropriate only
to certain pre-existing internal or external environmental conditions.
Wholes That Are Greater Than the Sums of Their Parts

Emergences are innovations that in their most radical form constitute new levels of
organized complexity. Their novelty comes from novel relationships among pre-
existing systems, combined perhaps with contingent catalytic additionsin lay terms
they produce wholes that are greater than the sums of their parts. For example, at the
molecular level the whole of a hemoglobin tetramer loads and unloads oxygen much
more efficiently than four separate hemoglobin monomers. This is because the
subunits, if separated, cannot cooperatively change shape to accelerate the process. At
the organismal level, such emergent wholes are well exemplified by endosymbioses
that generated eukaryotic cells with a constellation of new relationships. When mul-
ticellularity was generated it possessed only minor emergent properties. Yet the
differentiation of the many cells realized the Aristotelian concept of separation of
offices and the concurrence of efforts, which he compared to the harmonious
efficiency of a well-organized city state. Some emergences are not all-or-nothing
saltations of this kind, but may arise at critical points in continuities. For instance, if,
over many generations, continued allometric growth causes a continuous increase in
wing size, in an animal that can already flap and glide, there will be a critical point
where lift exceeds drag, and true flight emerges. This kind of emergence is quite
predictable from aerodynamic principles. But the biological pattern of growth that
reaches the threshold of flight is harder to reduce.
New organismal wholes obey the fundamental rules of physics, chemistry, and
biology, but their own novel emergent properties can override those of the lower hier-
archical levels. For example, the brains neural emergent property thought can override
reflex, such as a rush of hormones produced by an older emergent level. Emergences
create material wholes that are greater than the sum of their parts. For example, in
symbioses, a compound toxic to a host organism may be used by its symbiont to make
useful molecules. Emergences are a mix of the predictable and the unpredictable, as I
will establish in chapter 10. Since a higher level of organized complexity has novel
emergent qualities, the search for causal evolutionary continuity from the physico-
chemical up to the conscious is counterproductive. Because of emergent
discontinuities, a unified theory of the evolution of biological complexity will not be
found at the physical level. While a search for commonalities at all emergent levels is
desirable, the novel properties of each level require individual focus.
Key Innovations
Another word of caution: Biologists who have been trying to translate what I have
been writing about emergences into their own more familiar language are probably
asking Is he referring to key innovations? It is typical of Western epistemology to
particularize from a confusion of possible causes. So it is not surprising that to clarify
emergent evolution we might seek crucial, catalytic, novel phenomena that are the
keys to success in entering new environments, or to getting the jump on the
competition. It is also necessary to know all the generative conditions of emergence. They
amount to all of the molecular, organismal, and environmental qualities that are
necessary for an emergence to occur. These are roughly equivalent to the initial
conditions of cosmologists and complexity theorists.
Key innovation is useful for a generative condition that comes along later than
the others either as a crucial catalytic variation or a new contingency. New contingen-
cies are to be found in molecular, physiological, and environmental relationships, as
will become clear from examples in the following chapters. Key innovation can also
refer to a particular quality of evolutionary emergence. However, total focus on a
single crucial novelty is to see a tree and ignore the forest. For the qualities that result
from an emergence I am going to borrow the expression constellation of emergent
properties, a metaphor that several authors have already applied. Therefore, as well
as cautiously identifying key catalysts and key effects, I am going to attempt to
delineate the minimal requirements for generation, however many there might be.
And I will do what I can to sketch all of the consequent properties. There might be
84 Chapter 2
only one or two, if any, that are of immediate advantage, but they could not exist
without the others, and it is often the case that the others eventually participate in the
diversifying evolution that follows major biological emergences.
Evolvability
Modern selectionists, who have little constructive to say about adaptability and
progress, are now daringly asking themselves Does evolvability itself evolve?30 There
is a marked contrast between the answers of the Modern Synthesis and those of
emergentism; even the question itself has a different meaning in the two contexts. For
the selectionist it is axiomatic that natural selection causes evolution, so the question
means Does evolvability have selective advantage? Moreover, all that evolvability
means to a selectionist is the ability to generate potentially useful variations that can
be selected. If that is factored in, the question becomes Does the ability to generate
potentially useful variations have selective value? That simply returns us to the con-
ventional view of neo-Darwinism that genetic variety in a population is useful in
fluctuating conditions. And genetic variety need only involve a mosaic or
polymorphic population with an existent wide range of alleles. An underlying ability
to generate genetic novelty might be seen as a wasteful property that would tend to
be culled regardless of conditions.
The question of evolving evolvability demands more than an impoverished selec-
tionist answer. Something along the lines of macroevolvability or progressive
evolvability is wanted. To an emergentist, the answer starts with the emergent
properties of the first life forms. In addition to maintaining their integrity by being
adaptable organisms, they also had the evolutionary potential to become more
complex through multiplication. Prokaryotes could only try simple natural
experiments, and unicellular eukaryotes could only get a little more complicated. The
pace did not really pick up until sexuality and multicellularity originated, and it
accelerated yet again when terrestrial organisms with high metabolic rates and more
sophisticated feedback mechanisms emerged.
In other words, evolvability was itself an emergent property of the first simple
organisms, and in some lineages it has indeed evolved progressively at an accelerated
rate despite the obstacles placed in its way by the agents of natural selection. In this
light there seems to be a certain inevitability of evolution, making the word resonate
with its old meaning of unfolding. However, complexity was potentiated rather
than contained within the founding organisms, and neither a final predetermined
goal nor a predictable route is implied.
Emergentism and the Historical Theory of Evolution

Much of the evidence for the reality of the phenomenon called evolution remains
the same as it was in Darwins time, but a shift of interpretation comes with
emergentism. Evolvability is something that Darwin thought important, though the

previous section shows just how differently evolvability can be interpreted in the
context of progressive evolution. And emergentism treats evolutionary tempo and
speciation differently. For a start, they are treated as causally separate categories.
Beginning with a Bang

Evolutionary emergences may require long and gradual acquisitions of the appropriate
generative conditions, and yet occur almost instantaneously, as in the case of
endosymbiotic associations of prokaryotes. Some epigenetic emergences, although
subject to environmental influences, are fundamentally the result of molecular
changes that occur in fractions of a second, or cell movements that take only
moments, in marked contrast with gradual evolution on a geological time scale.
Indeed, the original cosmic Big Bang established all of the familiar physical rules for
the subsequent development of the Universe in a fraction of a second. Gregory
Benford writes:
The Big Bang would also be better termed the Enormous Emergencespace-time snapping into
existence intact and whole, of a piece. Then it grew, the fabric of space lengthening as time
increased. The crucial new element here is the vibrant role of space-time itself. This, ancient
Newton missed.31
Environmental change has often had an all-or-nothing, sudden impact as well, when,
for example, aquatic organisms emerged onto land, when climates changed rapidly, or
when bolides impacted. The Big Bang of Biology, as early Cambrian evolution has
been called, may not be measurable in microseconds, but the time scale of the
emergence of the relevant novelties may be measurable in tens of years, rather than
the tens of thousands of years proposed by the most radical of neo-Darwinist
punctuated equilibrists. The interpolation of periods of non-evolutionary stasis is
what brings the total lapsed time into the geological time frame.
Speciation
Darwinists believed that speciation was the product of adaptational divergences of
populations of an existent species, and that the establishment of new species was the
crux of evolution. There is now a spectrum of explanation that ranges from the
Darwinian position to the idea that speciation is a coincidental process that may not
involve adaptation until after new species are in place, and perhaps not even then.32
Although the species concept has undeniable practical value for categorizing
organisms, the species problem, as a taxonomic issue, could be a quaestio disputata
a How many angels can dance on the head of a pin? sort of question. It cannot,
however, be rejected, since it is interwoven with sexual reproduction and population
diversification.
86 Chapter 2
Bolder neo-Darwinists distinguish distinct kinds of speciation eventfor

example, the experiments in body plans conducted at the time of the Cambrian
explosion. These speciation events might be better called emergences, and they
cannot all be filed as Darwinian speciation and forgotten. The appearance of what a
taxonomist would call a new species is not a definitive step in evolution; it may only
be epiphenomenal to emergence. Reproductive barriers can be erected by geographi-
cal isolation, behavioral differences, capricious likes and dislikes within populations,
or by mutual sterility between populations. By protecting new types from genetic
dilution and incompatible hybridization, they are significant from any point of view.
But emergentism particularly recognizes the importance of preserving not merely
novel gene variants but unique organisms, along with their genetic and epigenetic
combinations. The emergent organism may found a new phylum or only a new genus,
depending on its emergent properties, and environmental contingencies that affect
subsequent diversification. Or, appearing in the wrong place at the wrong time, it may
be doomed to scant success or failure. But regardless of its evolutionary potential it
always belongs to a species. Eventually diversification will peter out into a number
of species locked into ecostasis.
Another consequence of reproductive isolation combines some of the features of
genetic drift and founder effect. If emergent types appear in a small population
through an unusual genetic combination that then increases through drift, such
creatures might realize their hopes by finding themselves in like company, and their
emergent properties will characterize their future lineage. Natural selection need have
no hand in determining the universality of those emergent qualities within the new
population.
Emergentism and the Causal Theory of Evolution

Although a real phenomenon, the syndrome of causes and effects known as natural
selection is not the cause but a consequence of natural experiment. Its agents hasten
specialization, and fine-tune epigenetic, physiological, and ecological homeostasis. In
so doing it has the positive role of consolidating the position of the new emergent,
and thus it parallels the role of normal science when new paradigms emerge. There are
several distinct categories of natural experiment that constitute the primary causation
of evolution. They are experiments in symbiosis and association; experiments in
physiology and behavior, and experiments in epigenetics and development. They
affect all hierarchical levels in the organism from the molecular to the whole organism
in its relationship with its environment. They all operate within internal milieux and
external environments, and interact through feedback and feedforward loops. The
operational details of these aspects of emergent evolution will be surveyed in the
following five chapters.
Natural Experiment as a Metaphor

This is subject to the same criticism as natural selection, i.e., that it seems to imbue
nature with purpose. Intention is not inferred in either case, but since such figures of
speech are easily abused, natural experiment needs clarification. An expression that I
began to use as a glib response to the selection metaphor, it requires more substance
if it is to stay the course. Nature has no intentions of playing scientist, selector, or
anything else, but changes occur, and they are not always random. Selectionists would
have no problem with the statement that the experiments involve spontaneous
changes in DNAthey would retort that natural selection takes care of the rest, and
thats all that needs to be said. Therefore the inadequacy of this oversimplification
must be exposed.
Natural laboratories exist in different places, at different hierarchical levels. The
biosphere is a heterogeneity of ecosystems, organisms, and their internal environ-
ments, cells, and molecules. In some of those laboratories, trials are less erroneous
than in others. At interfaces between environments, the accumulation of molecules,
or unicells, or multicellular organisms, make closer associations or symbioses more
probable. At the gene level, accidental changes in modifiers may result in nothing
significant in prokaryotes, but if they alter epigenetic programs in a developing plant
or animal they may have major consequences. If they are disintegrative they do not
count, and if they affect organisms by increasing their self-organization, they persist.
If they have adaptational qualities they survive and reproduce differentially. When
multicellular plants and animals began to differentiate, their interaction with each
other and with the environment at large generated specific instead of random
responses. Animals able to tolerate or accommodate to environmental change experi-
mented behaviorally. With more resilient homeostasis, they extended their horizons.
With more complex nervous systems they began to make choices.
In the previous chapter I agreed with Alfred Russel Wallace that artificial selection is
a bad analogy for natural selection. But to what extent does it provide a valid analogy
for natural experimentation, or for the laboratory where such tests are carried out?
Human control of plant and animal breeding emerged 10,000 years ago, and has
advanced considerably since then. It began with whatever improvements could be
obtained. Dogs that were tolerable, or even attractive for their tameness and
playfulness, were able to hunt and herd; they could also be eaten in a season of woe.
Domestic sheep and were first brought together on the basis of their natural herding
behavior, and goats may have been camp followers of early nomads. The first grains
were probably chosen consciously for their size and threshability. Natural qualities
beneficial to humans were both accidentally gathered and deliberately picked. Novel
broodstock organisms were brought together in the same place at the same time, and
competitors, predators, wild browsers, and random back-crossing with the wild
populations were excluded. Thus, protection from the agents of natural selection,
88 Chapter 2
enhancement of nutrition, and prevention of genetic dilution were guaranteed by the

action of the breeders. These conditions are all available in the natural laboratories of
new environments made available through organismal adaptability; and sometimes
nature, like Hercules, catastrophically cleanses the Augean Stables. But these are only
the circumstances under which experiments succeed. What generates the experimen-
tal changes themselves?
With some justification, it has been suggested that human breeders establish the
genetic propensity for change in their breeding populations through artificial founder
effect. Belyaevs Arctic fox broodstocks were not inbred, yet behavioral interactions
among them and their handlers could alter their reproductive patterns through
hormonal effects. This does indeed occur in nature. When it comes to adaptability,
protective artificial conditions can bring out exotic cognitive features in such animals
as dolphins, parrots, crows, and the great apes. Wallace was correct in thinking that
such dilettantine qualities would be quashed by natural selection. But we should go
further, to ponder the conditions where natural adaptabilities of physiology and
behavior could be generated, and not be quashed, but immediately flourish, or hang
on until propitious environmental changes occurred.
To fully realize the implications of this argument, we have to understand that the
whole of biospheric heterogeneity, and the interactions of its component organisms,
provide for natural experiment. Wherever we enter this whole, to analyze evolution
with our eyes open, we can see that local experiments have consequences that
reverberate throughout. Molecular breeders may have refined their selective artifices
to the actions of single genes, but to identify spontaneous mutations of DNA as the
generative causes of natural experiments is to deny the meaning of the rest. Thus, the
question put by John Holland (1998)What circumstances make the unlikely more
likely?does not have a simple answer. As well as a multiplicity of conditions that
generate the experiments, the nature of the laboratory determines their results.
Emergence and Environmental Contingencies

Emergences that result from natural experiments can be fully appreciated only in an
environmental context, whether in the internal milieu or the world at large. Some
environmental contingencies are biological, such as the availability of potential
symbiotic partners that can interact to form wholes greater than the sum of their parts.
The presence and population density of other conspecifics, or different species, can
stimulate developmental changes in some organisms. Other contingencies are random
physical events, such as change in climate, and catastrophes. However, some
conditions that await the progressing organism are fixed and predictable, such as the
availability of freshwater and terrestrial environments with distinct physicochemical
features: salinity, acidity, oxygen content, gravitational pull, and light intensity, for
example. This physicochemical heterogeneity of the environment may physiogeni-
cally change organisms as they move, accidentally or by choice, from one phase to
another.
Thus, some natural biological experiments are contingent on organism-
environment interactions. Conversely, some environmental conditions such as the
oxygenation of the biosphere are contingent on biological events. These geophysio-
logical adjustments support James Lovelocks Gaia Hypothesis.33 Other significant
environmental contingencies are random geophysical events, such as volcanic
eruptions, earthquakes, and the movement of tectonic plates. Like the cataclysmic
impacts of bolides, these can alter the course of natural experimentation and
evolution by clearing the bench for new trials.
Last First Words
Whats in a Name?
Emergence is the name of a process that may be non-biological or biological. It is
manifested as the sudden appearance of a new quality, sudden having a time span
ranging from microseconds to tens of years. The new quality results from a unique
combination of generative conditions. Some of these may be rare or unlikely; some
may already be in placeessential to the persistence of the complex pattern. Hence,
the run-up to the apparent leap may be protracted into geological time. The generative
conditions might build in a particular direction through self-amplifying mechanisms
interacting with habit and habitat. This too takes time, until a threshold is reached
where the new property emerges. If a strong dynamic stability prevails where a novel
emergent occurs, its presence may go unnoticed until that stability is undone. If there
is no resistant hypostasis the novelty will immediately increase in numbers.
There are four phenomena that distinguish biological from non-biological
emergences. The first is biological reproduction, which gives emergent patterns of
living complexity some guarantee of persistence, despite their thermodynamic vulner-
ability. That is linked to the second general quality of living emergents: dynamic
integrity. They are self-maintaining. Reproduction combines with integrity to add a
third emergent quality: the ability to conduct natural experiments in emergent
evolution. The fourth phenomenon is also experimental: organisms can match their
integrity against a variety of environments, and so induce both physicochemical and
biological changes in themselves. Increase in the complexity of organisms, or the
acquisition of new emergent qualities, equates with increasing freedom to direct
specific activities. Goal-directed sequences, from biochemical pathways to distinctive
behavior, finally contribute to purposeful action or inaction.34
90 Chapter 2
Emergence by Natural Selection

My opening broadside for an Emergence Synthesis asserted that natural selection,
though a real phenomenon, obstructs evolution. The selectionist counterattack is that
emergence, though a real phenomenon that they might reluctantly call macroevolu-
tion, is generated by natural selection. They claim that in populations, adaptive
alleles, and groups of alleles that interact to produce microevolutionary, adaptational,
phenotypic traits, are accumulated and concentrated through natural selection. This
increases the probability of combinations that constitute qualitative emergent change.
The dissonance of selectionist emergentism is illustrated in The Biology of Ultimate
Concern (1967) by Theodosius Dobzhansky, an evolutionist who frequently peered
beyond the hand of Darwin into the abyss. Instead of emergence, Dobzhansky used
transcendence, being careful to say that he meant a real phenomenon as distinct
from any kind of vitalistic essence:
The biological evolution has transcended itself in the human revolution. A new level or
dimension has been reached. The light of the human spirit has begun to shine. The humanum is
born.
It remains to consider briefly some of the misgivings which arise in connection with the above
account of the evolutionary transcendence giving rise to man. Those who see an unbridgeable
gap between the humanum and the prehuman state question the presence on the animal level
even of rudiments from which the humanum could arise. Now, the point which the believers in
unbridgeable gaps miss is that the qualitative novelty of the human estate is the novelty of a
pattern, not of its components. The transcendence does not mean that a new force or energy has
arrived from nowhere; it does mean that a new form of unity has come into existence. At all
events, no component of the humanum can any longer be denied to animals, although the
human constellation of these components certainly can.35
So far, so good, especially since there is still fierce debate over what humanness
actually is. Of course the generative conditions must exist in the pre-human state.
Dobzhansky prefaced those conclusions with the qualification that natural selection
is automatic, blind, . . . lacking foresight, [and] opportunistic. Accordingly, in
radical evolutionary reconstructions, the emerging product is an appalling mixture of
excellence and weakness. That this is the case with man is almost a platitude.36 Now,
I have already admitted that the syndrome of natural selection affects the processes of
internal and ecological adjustments that follow emergence, and lead to dynamic sta-
bilization. Yet immediately after his inspiring remarks on transcendent materialism,
Dobzhansky retreated back to selectionist romanticism:
. . . natural selection is in a very real sense creative. It brings into existence real novelties
genotypes which have never existed before. Moreover, these genotypes, or at least some of them,
are harmonious, internally balanced, and fit to live in some environments. Writers, poets,
naturalists, have often declaimed about the wonderful, prodigal, breathtaking inventiveness of
nature. They have seldom realized that they were praising natural selection.37
Natural selection does not bring novel genotypes into existence. Organisms bring novel
genotypes into existence. The existence of those organisms is not due to natural
selection. Their existence is due to the simple emergent qualities of life: self-
maintenance, self-organization, and reproduction. Competition and natural selection
are epiphenomenal to those, so the writers, poets, and naturalists in question had
not missed the point.
The gradual accumulation of good genes is a more recent variation of
Dobzhanskys error. It cannot be omitted as part of the process of emergence and its
consequences; yet it is a genocentric oversimplification. It overlooks the fundamental
similarity of all organisms at the DNA level. If selective accumulation of adaptational
mutant genes were responsible for major phenotypic differences, there would be
major DNA differences between ourselves and the bonobo, our nearest chimpanzee
relative. But we differ by only 1.3 percent. The selectionist argument refuses to accept
the saltatory nature of emergences, and the fact that the components of such interac-
tions have to be generated before they are selected. Nevertheless, in chapter 8 I will
offer the emergentistic selectionists another round of debate.
My argument that the success of evolutionary experiments is obstructed by
competition and predation has been heavy-handed, in order to make my point. And
some critics have remarked that there are many other routes that selection can take to
ensure the success of particular novelties, instead of their repression. My response is
that the origin of such adaptiveness contains its fate, making natural selection a
redundant concept. Therefore, understanding the origins and the qualities of novelties
is the way to understand evolution. As to the proof of the pudding, sample the courses
of associative, physiological, behavioral and developmental evolution that I am about
to serve, before deciding that the short commons of selectionism offer the more satis-
factory meal.
An Emergence Synthesis
In constructing the following list of contrasts between the emergentists and the selec-
tionists approach to evolution, I have taken a contrarian stance. But the fact remains
that differential survival and reproduction are measurable effects, and the agents of
natural selection include real biological phenomena. They cannot be omitted from a
complete synthesis. The chapters that follow immediately deal largely with the selec-
tionists proximate causes of evolution, and might be considered a contribution to what
Goodwin (1994) calls a science of qualities. Ultimately, however, we will be
confronted by the need to synthesize emergentism and selectionism, which will be
realized in chapter 11.
92 Chapter 2
An Emergence Formula
Until now, I have avoided the question of whether there can be a general formula that
applies at all emergent levels from cosmology through life to mind. The epigraph from
Cohen and StewartThere ought to be some kind of formal structure that captures
the essence of emergenceexpresses the complexity theorists wistful hope for the
grail of a universal formula. Holland (1998) establishes a way station for such a quest,
but his hopes are likely to be curtailed. Sol and Goodwin (2000) show that particular
emergent levels are open to mathematical formulation, but they note that because of
the non-linear nature of emergence itself, particular principles can neither predict nor
be sufficient to higher emergent levels. The great allure of emergentism to some reduc-
tionists that Corning (1998) mentions comes from wishful thinking that from the
mathematics of game theory, chaos theory, and non-equilibrium thermodynamics will
come a predictive formula that will finally conquer the messiness of life. It is a false
hope.
The progressive evolution of a particular lineage might very well be made to fit a
theoretical curve based on a simple equation in which increased complexity is a
function of reproduction and differentiation in time. But we should not make the
same error as Lamarck, about evolutionary progress being a simple time function.
Although all life increased in complexity to some degree, in many evolutionary lines
it ceased or regressed, and where it did not, its progress was irregular. Even if lineages
that ceased to progress, or became extinct, are ignored for the sake of clarity, a simple
curve of progressive evolution still could not project the irregularity of saltatory and
critical-point emergences. And although causal contingencies might be expected, only
hindsight allows them to be identified and placed on the curve. Therefore, even if
such a general unifying formula could be approximated, emergence is such that a
perfect knowledge of biological origins could not contain or predict the particular
nature and timing of future evolutionary novelties. Life emerged in a universe whose
cosmology is subject to physical laws. But life, without disobeying such principles, is
not predicted or contained by them. One apposite developmental problem is
pinpointed by Walter Gehrings description of his quest for determinants of anterior
and posterior structures in Drosophila larvae. A mathematical model of segmentation
based on the Turing reaction-diffusion equations required only one determinant. But
Gehring discovered two; he had not been chasing a ghost:
. . . in this case nature did not find the most parsimonious solution. As we shall see, evolution
requires a lot of tinkering, redundancy, and double assurance, that only later is streamlined
through natural selection.38
While the quest for a generative theory of emergent evolution may be arduous, it must
begin with the first step. That it is directly relevant to evolution rather than to its
demographic consequences is a start. Putting life, mind, the organism, progressive
Table 2.1
Emergentism Neo-Darwinism
Addresses the causes of evolutionary Ignores the causes of evolutionary innovations.

innovations.
Addresses progress, which is equated with Ignores progress. Subsumes adaptability under
adaptability and increased complexity. adaptation. Doesnt like complexity.
Combines saltatory and gradual processes. Denies saltatory processes.
Natural selection is an obstacle to evolution. Natural selection is the cause of evolution.
Includes autonomous organismal cause. Denies autonomous causes.
Stresses importance of organisms, and Stresses importance of populations as gene
populations as made up of individuals with pools, and reduction of phenotypes to selfish
unique phenotypes. genes.
Environment directly affects physiology, Environment only sets conditions for
behavior, and development. adaptation.
Biological changes at the organismal level Genetically heritable changes are the fount of
precede genetic fixation. evolution by natural selection.
evolution and freedom back into theoretical circulation should have some restorative
effect along the way.
Table 2.1 summarizes the dissimilarities between the neo-Darwinist Modern
Synthesis and an Emergence Thesis.
Natural selection is an obstacle to evolution is more dramatic than punctilious.
Evolutionary change can occur anywhere at any time. It is on the whole a random
process, although I will be narrowing down the generative conditions for emergent
evolution to those that are the most likely. What natural selection, or the stasis that it
reinforces, actually obstructs is not qualitative evolutionary change, but the successful
establishment of emergent novelty in sufficient quantity to make the kind of impact
that might feature in the fossil record. Such establishment is due either to superior
competitiveness, in which case it is wrongly subsumed as an effect of selection, or to
freedom from competition.
Commonalities of Emergentism and Neo-Darwinism

Speciation is not a pivotal event of evolution in my brand of emergentism.
Nevertheless, I share with neo-Darwinism the concept of speciation as a ratchet pin
that prevents regression of novelty through genetic dilution by interbreeding with the
older forms of organisms. It is also an inevitable concomitant of emergent qualities
that permit population expansion and diversification.
Evidence for the historical reality of evolution is similar in both theses, but its
tempo, patterns and modes are subject to different interpretations, as demonstrated in
94 Chapter 2
the above discussion of how emergentism affects the historical theory. Emergentism
has the potential to resolve and rise above the present crises of evolutionary thought.
Antonio Lima-de-Faria (1986) presents an extensive table of differences between his
autoevolution and neo-Darwinist evolution with which I largely agree. However, my
immediate goal is to keep the contrasts simple, and to broaden them later in chapter
10.
A more leisurely exploration of generative emergent causation follows, and by the
time we get to chapter 8 we should be in a better position to assess its formal require-
ments as well as its limitations. We are going on an intellectual field trip, and the first
part of the quest is a visit to the evolutionary circus. There are bound to be a few thrills
and spills, but dont panic! You are in good company. The faint-hearted went back
home before the end of the last chapter, and never even got to the ticket office. As far
as the circus is concerned, you might want to watch out for the following:
mechanisms common to all causal arenas
the generative conditions from which emergences spring and any features common
to them all
factors that catalyze emergences, provided that appropriate setting of generative

conditions is in place
particular contingencies, predictable or unpredictable that have affected generative

conditions and the success of their emergences
the adaptable constellation of multiple properties characteristic of new emergences
the course of emergent evolution that has progressively led to greater self-organiza-
tion, independence, and freedom of choice.
I make no apology for my zoological and anthropocentric bias in the last of these
points.
The field trip has a shortcut. The traveler who doesnt have the experience to
appreciate the performances, or the endurance to tolerate the sweat and the
greasepaint at the three-ring circus, can pick up the rest of the expedition at the exit
of chapter 7, and continue with the quest in chapter 8. chapter 9 reviews the major
circus performances, and leads into the goal which I hope you will find in chapters 10
and 11.
Bon voyage!
3
Evolution by Association
Symbiosis, like sexuality, is a powerful force that has brought together preadapted genetic com-
binations, at least initially, in the absence of mutation. Symbiotic complexes are important
sources of raw material for genuine evolutionary innovation.
Lynn Margulis, 19811
From the long view of geological time, symbioses are like flashes of evolutionary lightning. To
me symbiosis as a source of evolutionary novelty helps explain the observation of punctuated
equilibrium of discontinuities in the fossil record.
Lynn Margulis, 19982
If it is indeed in social organization that we find emergent evolution most manifestly at work . . .
then we shall be cautious in accepting even the advice of the king of the termites on our own
social problems.
H. S. Jennings, 19273
Association and Emergence
Associations within and between organisms are the alpha and omega of evolution:
involved in the emergence of life and in the latest adjustments to human culture. In
the early stages of life on Earth, symbioses altered the biosphere and established major
ecosystems. Such associations emerge quickly and generate new wholes that are
greater than the sums of their parts. Therefore, it is not surprising that Lynn Margulis
invokes discontinuity of innovation. Yet the first epigraph misses one fundamental
point: Symbioses are not simply important sources of raw material for genuine evo-
lutionary innovation (as if they had to wait for natural selection to approve before
they actually evolved)they are in and of themselves genuine evolutionary
innovation.
One of the natural experimental processes that Margulis discusses is a mix-match
principle that applies to associations at many levels of organization, from molecules
96 Chapter 3
and cells to organisms and societies.4 That can be complemented by the concept of
repetitive differentiation, whereby existing units are multiplied, varied, and re-
associated in novel groupings. Life emerged when organic molecules mixed and
matched in competent combinations. Primitive cellularity came from protobiont coa-
lescences. Exons, the functional subunits of genes, can also be mixed and matched to
produce a variety of proteins. Also, protein domains, once they have been synthesized
according to the exon codes, can be mixed and matched to make novel protein
molecules.
Intimate endosymbioses of prokaryotes gave rise to the eukaryotic cells of protoctis-
tans, fungi, plants, and animals. When eukaryotic cells formed multicellular
associations, they could then differentiate and undergo epigenetic evolution. Logically
and chronologically, the causal arena of evolutionary association claims priority for
consideration as a major component both of a generative theory of evolution, and of
the new biological synthesis that is needed to replace the Modern Synthesis.
As Margulis infers, protosymbionts, as independent organisms, already had their
own genetic systems, functionally attuned to their independent modes of life. Then,
the sudden intercourse of two different genomes and cell types generated a broad con-
stellation of emergent properties. This flash of evolutionary lightning contrasts
starkly with eons-long accumulations of adaptational mutations. The component
organisms of symbiosis were preadapted only in the sense that they already formed
functional wholes that could persist in their own being. But in endosymbionts they
had novel properties that arose from complementarity. Margulis puts it plainly in the
language of emergentism: The tendency for independent life is to bind together and
reemerge in a new wholeness at a higher, larger level of organization.5 Endosymbioses
that gave rise to eukaryotic cells clearly demonstrate progressive and saltatory change.
Nevertheless, emergent symbioses may be more fragile than their formerly
independent constituents, and subsequent adjustments are needed to reach the most
dynamically stable state, where homeostatic flexibility is achieved with minimal
energy output.
Once multicellular eukaryotic foundations were laid, epigenetic evolution could
build upon them through intercellular and sexual associations. Thereafter, symbiotic
interactions between individual organisms continued to make intermittent but major
contributions to the complexity of the biosphere by founding new ecosystems. Social
associations within and between individual species of insects, birds and mammals
made further evolutionary emergences and divergences possible.
Despite a growing trend among biologists and psychologists to reduce the properties
of associations, including human society, to genes, emergentists have always
understood that every evolutionary emergence contains novelties of organization that
were not in the simpler levels, and were therefore not predictable from them. Herbert
Spencer Jennings, quoted in the third epigraph to this chapter, cautioned particularly
Evolution by Association 97
against extrapolation across phyletic gulfs, from organisms such as social insects
whose behavior is extensively gene-based, to humans whose behavior is largely
cognitive. By including all of the different kinds of association in one chapter, I hope
to construct a minor synthesis of associative evolution that fits the framework of
emergentism. However, intercellular association in multicellular organisms is largely
in the developmental arena, and will not be elaborated in this chapter.
Decoding the Terminology of Associations
In Evolution by Association (1994), Jan Sapp notes that A. B. Frank (1877) coined
symbiosis for close interspecific relationships, excluding parasitism. The following
year, de Bary broadened the definition to include parasites and societies, and he also
implied that the evolution of symbioses did not require an active role for natural
selection. The title of Sapps book avoids semantic ambiguity, and he keeps it simple
by omitting intercellular associations, sex, and social interactions.6 However, despite
serious attempts at formal definition by others, usages still vary. Some modern
biologists prefer mutualism for symbioses in which both host and guest benefit. Yet
mutual advantage is implicit in endosymbiosis, the most intimate kind of association.
Symbiogenesis is used for the emergence of symbiosis.
The term symbiont is used for the organism that takes up residence in a host. Yet
there is no single word for the combination of host and symbiont. Margulis uses
symbiotic complex and occasionally refers to a chimera. Composite,
consortium, and association are useful general terms, but they miss the symbiotic
nature of the complex. How about reviving the word symbiote for the symbiotic
whole? Sapp cites the discussion of the Committee of Terminology set up by the
Society of Parasitologists in 1933.7 They concluded that the choice of terms was a
matter of taste and usage rather than of correctness. They discarded symbiote over
the objections of their philological consultant, and chose symbiont as a word that
could apply to either member of the symbiosis. Symbiote and symbiont
continued to be used interchangeably, for a while, but scientific usage now favors
symbiont for the smaller member of the complex; symbiote appears more
frequently in science fiction. I do not like to neologize, but I am going to use
symbioplex as the obvious combining form of Marguliss symbiotic complex. Ill
try not to overdo it.
Some symbioses put a curious twist on the inheritance of acquired characteristics. In
my 1985 essay Unpredicted factors of evolution: The theory of emergence revisited,
I used the acquisition of heritable characteristics for emergences involving gene
transfer or genome pooling between previously unrelated organisms. My purpose was
to draw a distinction between the phenomenon and the conventional interpretation
of the Lamarckian inheritance of acquired characters. Eugene and Elisabeth Wollman
98 Chapter 3
first appreciated this distinction in 1925, and they called it paraheredity.8 In

Evolution: The Modern Synthesis (1942), Julian Huxley had already used allopoly-
ploidy for the combination of karyotypes (chromosome complements) by
hybridization in plants. Lynn Margulis and Dorion Sagan (2002) now refer to these
kinds of combinations as the acquisition of genomes in their eponymous book. The
familiar modern expression gene acquisition implies an extrinsic source for new
genes. It applies to the natural transformation and conjugation experiments routinely
conducted by prokaryotes, where genes are the major cellular components acquired.
The word symbiosis means an association involving two or more different species,
and is the kind of relationship that has priority in this chapter. However, intraspecific
associations are involved in sex, multicellularity, and societies. These will therefore be
included in the following outline of the categories of association.
Interspecific Associations
Endosymbiosis
This signifies an intracellular association, such as the presence of mitochondria in our
own cells, and the additional acquisition of chloroplasts by plants. Viruses, bacteria,
algae, and fungi may be also be found in the cells of multicellular organisms, and on
occasion the symbionts have their own lesser endosymbionts within them. In
endosymbioses there is not only an exchange of energy and molecules between the
symbiotic cells, genes have been transferred, resulting in a near monopoly of protein-
synthesizing information by the nucleus. The mitochondria and plastids have also
had host translocation proteins inserted in their membranes, such that metabolite
transfer is facilitated.
Many endosymbionts are holobioticpassed vertically from one generation to
the next in the ova.9 They are not re-introduced from a pool of free-living,
independent microorganisms in every generation. Some symbioses involve
horizontal transmission, which means that the symbionts are not carried in the
eggs, but can exist as independent organisms and re-invade the next generation of
hosts. For example, when gardeners plant peas and beans they help establish a
symbiosis by applying a commercial soil inoculant of Rhizobium bacteria that enter the
seedlings, and then fix nitrogen for the synthesis of amino acids and proteins. The
dinoflagellate symbionts of corals are endosymbiotic in the digestive epithelia; but
they can be released into the sea to be horizontally transferred to juvenile corals.
In a less intimate association the symbiont may live extracellularly within the host
organism. Such symbionts may be passed vertically on the surface of the ovum, or hor-
izontally, entering the larva or juvenile from a nearby symbiotic source. Like corals,
giant clams have dinoflagellate symbionts belonging to the genus Symbiodinium.
Indeed the clams probably acquired the symbionts from corals in the first place. As in
the case of the corals, the clam larvae have no symbionts at first, but after a few days
of juvenile growth they obtain them from the seawater that they have filtered. The
source of these free-living planktonic dinoflagellates is incompletely digested fecal
matter from adult clams in the same vicinity. When they are eaten by the juvenile
clams the symbionts are not digested, but take up residence in translucent extensions
of the digestive gland that extend into the blood sinuses. Thus, they are extracellular,
and not intracellular, as in the corals. There are a variety of strains of Symbiodinium,
some of which are preferred by juvenile corals and some by juvenile clams, and if
several are acquired, only one succeeds.10 This reinforces two points: loose symbioses
can be precarious, and under competition only the most compatible strain of
symbiont is established.
In lichens, algae are associated with the fungi that make up the main structure, but
the different cells do not interpenetrate. The reproduction of both algae and fungi is
largely vegetative. Sorediasmall bodies that may be released from the parent
plantcontain both of the symbiotic partners, and establish independent lichens.
Sexual reproduction can occur in the fungus, resulting in characteristic fungal fruiting
bodies. This kind of symbiosis has evolved independently many times between
different algae and fungi. The ability of fungi to acquire mineral salts, combined with
algal photosynthesis, is greatly to the advantage of the symbiotic whole, and the algae
may be protected from browsers by fungal toxins. Where blue-green prokaryotes are
present they contribute nitrogen fixation.11 Lichens are characterized by a physiolog-
ical resilience that allows them to live in barren terrestrial environments where water
and mineral nutrients are scarce. Many are cold-hardy. Since the fungal pigments
protect the algae from damage by ultraviolet light, lichens may have been the first
plant-like organisms to successfully invade dry land, and once there they prepared it
for other plants by making soil.
Thus far, these have been examples of physically intimate, mutualistic associations
in which both partners exchange nutritive or other services. Other associations can be
very loose; their benefits may relate to nutrition, defense, or reproduction. For
example, some sea anemones that attach to the shells of hermit crabs eat fragments of
the crabs food, and protect them from predators with their stinging cells. They may
also extend the original shell apertures, saving the growing crabs from the trouble of
having to find a larger home. There are numerous cleaning associations where the
cleaners keep the hosts tidy by browsing on their epifauna, and they may also share
in their meals. In the sea, prawns and fish are common cleansers of larger fish, and on
land birds often provide the service to larger mammals and reptiles. These relation-
ships merge with commensalism, meaning eating at the same table, referring to
animals that lead separate lives but share their food, and perhaps a degree of mutual
protection.
100 Chapter 3
Some species domesticate other species. Not only humans keep house plants, pets,
farm animals, and crops. Ants, for example, often supervise the behavior of aphids,
milking their honeydew (sugary fecal secretions). Invariably, organisms interact
intra- and extra-specifically in their particular community, or subsection of their
ecosystem. Another generalization about societies that is useful in many contexts is
Aristotles aphorism that all collective life involves the separation of offices and the
concurrence of efforts.12 He not only discussed how this can be effectively achieved in
human society, but also applied the model to the coordinated functioning of human
functional anatomy.13
Human social and cultural evolution does not arise from the accumulation of
behavioral adaptations, but from the adaptability of our species. Adaptability is a con-
stellation of qualities that are physiological and behavioral, with links to
development. Adaptability allows the organism to respond effectively to changing cir-
cumstances. It makes the human organism a generalist rather than a specialist. And
although adaptability is grounded in the genes, it operates at higher levels of organi-
zation, and can vary from individual to individual and group to group in its
expression. The ultimate biological manifestations of that adaptability appear in the
central nervous system, the brain, and the conscious and subconscious mind. These
are what free us from the automatic responses of our primitive ancestors. All kinds of
association, whether intimate endosymbioses, or happy families, are sources of
emergent adaptability, and to seek their explanation at the level of the structural gene
is futile.
Symbiocosms
Terrestrial and aquatic biotopes are often composed of mosaics and mixes of different
symbioses that demonstrate a degree of interaction far beyond simple cooperative,
competitive and predator-prey relationships. These group relationships have been
called symbiocosms.14 As an erstwhile student of digestive physiology I have always
been interested in the mixture of cellulose-digesting micro-organisms that occur in
cattle, and in insects such as termites. However, a remark by microbiologist Lee Haines
refocused my attention to non-cellulolytic symbioses in insects, and extended it to the
literature concerning symbiocosms. She called the tsetse fly, Glossina, which she
studies, a soup of symbionts.15 Tsetse is best known as a vector of trypanosome
parasites that affect humans, their cattle, and game. Thus, its medical and economic
importance has made the full exploration of its symbionts desirable. The bacterial
symbionts include Wigglesworthia glossinidia, found in the cells of the bacteriome, an
organ composed of expanded epithelia of the foregut. Another endosymbiont, Sodalis
glossinidius, is found in the cells of the mid-gut. A third endosymbiont, a species of
Wolbachia, occurs in the cells of the ovaries, milk gland (part of the reproductive
system), fat body, and hemolymph. The first two endosymbionts have a mutualistic
relationship with the host, providing essential nutrients not contained in the blood
diet of the insect. They, in turn, benefit from the energy resources of the host. If they
are absent, the insect is unable to reproduce successfully.16 Wolbachia is more of a
parasite than an essential endosymbiont, and can have deleterious effects on repro-
duction. All of these microorganisms are transmitted vertically via the eggs. Thus, the
term symbiocosm could be extended to include organisms such as the tsetse fly.
The presence of endosymbionts is universal in insects that are specialized feeders on
plant juices and blood. The emergence of Aphidoidea, the aphids or greenflies, at the
end of the Permian, c. 250 MYA (million years ago), seems to have been triggered by
the acquisition of Buchnera, a proteobacterial symbiont that could compensate for the
deficiency of essential amino acids in plant saps.17 Minor bursts of diversification
within the aphid order can be traced to the acquisition of additional endosymbionts.
There is a strong correlation between the evolution of symbionts and their hosts,
which can be mapped quickly by identifying DNA base sequences, or protein primary
amino acid sequences, and comparing these to gene and protein databanks that have
accumulated since the human genome project was initiated.
The focus of my interest in the symbiocosm was our greenhouse, when our
aubergine plants became infected by aphids. (This is in the target-of-opportunity
tradition of T. H. Huxley, who ventured only once into entomology: when greenflies
infested his Pelargonium.) The aphids were placed on the aubergines by ants of the
species Lasius alienus that had found pastures new for their cows. They then
proceeded to feed upon the honey-dew that the greenflies exuded. Ants too have
endosymbionts, some being Buchnera strains, with which they were most likely
infected via aphid honeydew. Formica, and the wood ant Camponotus have endosym-
biont strains of the genus Blochmannia, which is related to Wigglesworthia. Wolbachia
is widespread among the entire family of the ants.18
Our greenhouse symbiocosm also has a population of ant lions, the larvae of
Myrmeliontidae, which are related to lace-wings. Their adults could be mistaken for
damselflies by non-entomologists. But the squat bodies, relatively enormous jaws, and
menacing behavior of their larvae are better known, since they have become models
for science-fiction monsters. They make ant traps in fine, dry soil or sand, and lurk
under the surface of the bottom of the pits. (The ant lions seem to have figured out
Per Baks collapsing-sand-pile problem a long time before he did.) When ants fall into
the pits they cannot get enough purchase on the loose substrate to escape, and by
flicking sand at them, the ant lion makes it harder. Then its bite injects a poisonous,
paralyzing saliva. The toxin secreted by the ant-lion endosymbiont Enterobacter
aerogenes is a homologue of GroEL, a variant of chaperonin, one of the heat-shock
proteins.19 Curiously enough, homologues are also found in aphid endosymbionts,
but they clearly have no anti-ant action.20 Toxicity relates to neural blockage, probably
by binding of the molecule to nerve cell membranes, and not to the original
chaperonin function.
102 Chapter 3
Another greenhouse pest from which our succulents and cacti suffered is the
mealybug, a species of Pseudococcus, an aphid relative. One of the South American
species of mealybugs has attendant silvanid beetles that solicit their honey dew.21 For
some years it has been known that the polyploid cells of the intestinal bacteriomes of
mealybugs have endosymbionts that provide essential nutrients. But now it is
discovered that those endosymbionts contain other endosymbionts. These could be
parasitic, but the researchers suggest mutualism.22
The Pacific coast termite Zootermopsis angusticollis was resident in the wood flooring
under some of the greenhouse benches. Termites have long been known to possess cel-
lulolytic bacteria and protoctists as well as nitrogen-fixing bacteria. In some of these
insects, symbiotic nitrogen fixation might equal that of free-living bacteria in the
same environment.23 Symbiotic filamentous fungi are present in the guts of some ants
and termites.24 The leafcutter ants, genus Acromyrmex, which make leaf-litter gardens
in which they grow fungi, also carry the spores of the fungi in their guts. These are in
addition to a wide spectrum of bacterial endosymbionts.25 The cuticles of some fungal-
gardening ants also bear Streptomyces, which are actinomycete prokaryotes that protect
their fungal crops from the parasitic fungus Escovopsis. As a bonus, Streptomyces also
produces growth stimulants for the ant-garden fungi.26 Coincidentally, various species
of this genus produce antibiotics that are widely used to treat human diseases.
A less common, but still unwelcome visitor to our greenhouse tomato plants is the
whitefly Bemisia tabaci. It not only feeds on the plant sap, it also vectors the yellow
leaf curl virus. Its symbiont Sodalis produces a chaperonin that is believed to protect
the virus from attack by proteolytic enzymes during its passage through the whiteflys
gut.27 Another of our plants, Abutilon pictum, a mallow that is sometimes called
flowering maple, is permanently infected by viruses. In this case the viruses do no
harm, but cause a leaf color variegation that has been deliberately selected by horti-
culturists.28 We feel that the micro-ecosystem of ant society and insect-bacterial-viral
symbioses truly elevate our greenhouse to the status of symbiocosm.
Co-evolutionary Associations
Some present-day biologists argue that from the evolutionary point of view the most
appropriate catch-all term for biological associations is co-evolution. Taken literally,
this is perhaps legitimate, but the classical instances of co-evolution involve different
organisms that live independently of each other much of the time, while influencing
each others adaptations through a literal selection process. Therefore, I will persist in
using association for the most general category, and I will use co-evolution in its
traditional sense (referring, for example, to the co-evolution of flowering plants and
pollinators). While this appears to be a literal instance of natural selection, plants with
flowers had first to emerge before they could be directionally selected for exaggerated
colors and scents by potential pollinators. Once specialized, flowers only permitted
pollinators of anatomical proportions suitable for carrying pollen to other members of

the same plant species to reach the nectar. There are, moreover, exploiters who simply
bypass mutual selection by biting into nectaries from the outside. The constraints on
these co-evolutionary arrangements re-emphasize the limitations of selection, both
metaphorical and literal. No novelty is produced; existent types are modified and
specialized until they have gone as far as they can go, and to get there they may have
been driven by molecular mechanisms that were indifferent to natural selection.
Symbioses may be precarious. In adopting symbionts or co-evolving with others,
organisms make themselves hostages to fortuneharm to one is harm to both. The
unicellular flagellate Euglena can digest its green symbionts in times of need, but in so
doing it loses photosynthesis and may not get it back again. When the Cretaceous was
terminated by an impacting bolide, near-extinction of the flowering plants was
probably affected by the near-extinction of their insect pollinators. However,
symbionts safely tucked away inside host cells are better able to meet such challenges.
Parasitism
Parasitism is occasionally lumped with symbiosis, but it deserves a separate category
since only one participant gains advantage, and the host is adversely affected.
Parasitism is, however, an interesting evolutionary association in its own right,
perhaps involving environmentally effected metamorphoses. It also illustrates just
how radically morphogenesis can be altered. For example, the crustacean parasite
Sacculina starts out as a normal nauplius larva, but once established in its crab host it
becomes a pervasive amorphous mass of tissue like fungal mycelium. Furthermore, the
complexification of life cycles and the proliferation of intermediate forms found in
parasites shows how high are the energetic costs of such precarious associations.
Viruses are parasites of a kind that can have highly disruptive effects on whole
species and ecosystems. They have co-evolved with their hosts, and sometimes
migrated to others where their deleterious effects were magnified. But they may also
contribute to saltatory emergences, since retroviruses can introduce foreign genetic
material to their hosts. We know about this mainly from genetic alterations of
bacteria, but some instances involve viral transgenesis between distantly related
vertebrates. Because of technical difficulties, it had not been possible to assess just how
widespread the phenomenon is. However, the recent completion of the human
genome project indicates which genes have been introduced by retroviruses, and
many bacterial genes have been found as part of the human makeup (as opposed to
the totality of genes that originated with the ancient prokaryotes in the early lineages
of eukaryotes).
Some of those retroviruses may have entered into a more intimate and non-patho-
logical association of virus and host. Endogenous retroviruses (ERVs) of mammalian
cells are now part of the mammalian genome, and the most familiar ones function in
104 Chapter 3
placental development, either in implantation or in preventing the maternal immune

system from rejecting the placenta.29 These kinds of retroviruses mutate much faster
than the host genes, and so have a greater potential to increase genetic variability.
Intraspecific Associations
Sex
Much ink has flowed on the subject of the evolution of sex and its selective
advantages; less will flow here. Sex brings organisms together; it would not be
stretching the category too far to say that the diploid sexually reproducing organism
is a symbiosis of haploids derived from two different parents. For the act of fertiliza-
tion, sexual associations are sometimes loose, and temporary associations, sometimes
in permanent proximity. Some female invertebrates and fish go so far as to carry quasi-
parasitic dwarf males around with them all the time. Sexual associations have many
physiological and behavioral implications, depending on the evolution of intercellu-
lar messengers, and the organs that produce them; attractants that range from
molecules to epidermal color patterns, enticing secondary sexual organs, and
behavioral modifications. Therefore, the evolution of the nervous system has also
been involved.
Sexual reproduction is also a major source of variability, and is therefore one of the
significant experimental evolutionary processes of nature. Its effects on the relation-
ships between organisms can be detrimentalmating dogs are oblivious to motor
vehicles. However, family associations correlated with sex have had an important evo-
lutionary role, especially in the vertebrates. Sex among the higher land plants is
sometimes called a better adaptation to the dry terrestrial environment in the sense
that their gametes are less prone to desiccation. Yet the fluid transportation
mechanism of animal gametes has required the very close associations that have had
so many evolutionary consequences.
Sex and Chromosomes

Before the different kinds of founding eukaryotic cells went off to find their fortunes
and establish their kingdoms, they had had already acquired the talismans of mitosis
and meiosis. Chromosomes are necessary both for the equal distribution of DNA
between daughter cells during mitosis, and also for the production of gametes by
meiosis, as the preliminary stage of sexual reproduction. The precursor of the
chromosome was the prokaryote genophorea large loop of double-stranded DNA,
which is normally a tangled mass. Unlike the eukaryotic chromosome, it has is very
little protein associated with it. The genophore carries the genetic information for
making essential structural proteins and enzymes. Prior to the fission of the cell the
genophore is duplicated, and usually two identical cells are produced. Prokaryotes
reproduce asexually, replicating themselves along with any genetic changes that have
occurred in them. But the primitive eukaryotes had several genophores and plasmids
from various symbiontsthe complexity of the eukaryotic genome had increased to
the point where packaging was crucial. Did one of the original symbionts become the
eukaryotic nucleus, and sequester genetic material from the other members of the
association? The following segment on chromosomes is largely based on Origin of
Eukaryotic Cells (1970) and Marguliss subsequent publications.
Eukaryotes have multiple chromosomes that usually consist of histone proteins,
bound to DNA, arranged linearly along them. There is also satellite DNA at the ends
of the chromosomestelomeresand in the centromeres, which control mitosis and
meiosis. Telomere attrition occurs in proportion to the number of times the cell line
has undergone mitosis, and this diminution may be correlated with senescence.30
Chromosomes have multiple functions, such as helping to regulate the expression of
their genes. In a multicellular organism the functions of differentiated cells require the
repression of most of their chromosomal DNA. Chromosomes also ensure to some
extent the preservation of whole organismal properties based upon a hierarchical
polygenic organizationalleles are not randomly mixed when gametes are formed.
Also, by condensing into compact rods during mitosis and meiosis, their spatial distri-
bution is easier to control. Imagine trying to shuffle and deal a deck of cards whose
individual lengths are proportionate to their numerical value. The long, tangled
threads of the interphase chromosomes have to be reduced to manageable units for
consistently even dispersal.
When endosymbiotic experiments were being initiated by primitive prokaryotes,
redundant DNA must have constitutively churned out proteins and wasted energy and
molecular resources. Regression and differential expression required differential
histone binding and methylation mechanisms, which were part of the shakedown
into dynamic stability. However, they were flexible enough to allow subsequent
change, and major steps in the direction of chromosome evolution and epigenesis.
In protoctists there is a variety of ways of dispersing DNA evenly, if not absolutely
equally, between daughter cells. The cell can make multiple copies of DNA and take
the chance that each daughter cell gets at least one complete set. The ciliates have
meganuclei that do the protein-synthesizing work of the cell, and multiple
micronuclei that carry sets of DNA that exist for reproductive purposes only. There are
also some variations on the theme of a mechanical spindle that pulls the
chromosomes apart during mitosis. Although animals have spindle-organizing
centrioles, and plants do not, the mechanics of mitosis are similar. There is no good
evidence to support the idea that the framework of moving spindle fibers originated
with ancient chromatin, i.e., the protein and nucleic acids of the chromosomes.
Instead the spindle apparatus came from an independent source, perhaps the
106 Chapter 3
symbiotic spirochete-like prokaryote. The basal bodies, or kinetosomes of locomotory

structures, such as flagella and cilia, collectively known as undulipods, contain their
own organizing chromatin which can generate both undulipods and mitotic spindles.
Ciliated cells in the bronchi of the lungs for example, do not mitose, because the
kinetosome is completely committed to undulipod function. When these cells wear
out they have to be replaced through mitosis of unciliated cells whose daughter cells
then differentiate cilia.
The division and separation of the basal bodies of the flagella/cilia could have
originated the spindle that pulls the chromosomes apart. Did spindle and centromeres
co-evolve, so that the attachment of the chromosomes and the separation of the
chromatids could be consistently effected? It is a more parsimonious idea than the
older hypothesis that proteins called tubulins, which form into microtubules, were
universally distributed from a common ancestor. There was then independent
evolution of undulipods, basal bodies, centrioles, and spindles in various evolutionary
lines, giving rise to different kinds of undulipods. Microtubules constituted functional
structures such as animal muscle fibers, as well as many other cellular kinetic
functions in all of the kingdoms of organisms. Whichever hypothesis is right, and
Occams razor shaves the options down to the Margulis-Sagan version, both are com-
plemented by the idea that the chromosomal centromeres, and spindle organizing
elements could have arisen from the replication origin and terminus of the prokaryote
genophore, where it attaches to the cell wall.31
That seems a reasonable argument for the derivation of the centromere, but what
about the centriolesthe bodies that participate in spindle formation? The endosym-
biotic version accounts for those as well, as part of the constellation of emergent
properties of the thermoplasma-spirochete symbioplex. The microtubular apparatus
emerged only once, originally as a locomotory system, but diverged in function to
become a spindle apparatus for host cells that had built up a nucleus with duplicated
genophores, derived from several symbionts.
Equal division might have been possible as long as the genophores remained few
and small. But chromosomes could be enlarged if they acquired proteins that could
condense and reduce them to manageable proportions for reproduction. These
emergent protein structures had the potential to regulate gene expression in future
multicellular lineages as well as condensing the chromosome structure. When mitosis
occurs in a cell some internal structures, such as the microtubular cytoskeleton and
internal membranes, including the nuclear membrane, break down and leave the cell
as an unobstructed stage for the dance of the chromosomes. Then they are all recon-
structed when mitosis ends. Even speculation about the evolutionary details of such
molecular events boggles the imagination. That a hopeful monster of a cell leaped into
existence with everything simultaneously in place is out of the question. As the
gradualists argue, we have to look at everything step by step. But the steps are
themselves saltatory emergences, and identifying their advantage does not explain
their genesis. Once the proto-eukaryote had assembled a useful complement of
chromosomes that could be equally divided among its daughter cells, it could then
clone itself in a stream of copies. Populations of the new eukaryotes would all have
consisted of very similar organisms. But finally the associative emergence of sexual
reproduction provided for greater experimental variability.
With chromosomes and mitosis in place, sexual reproduction was a comparatively
simple emergence. Diploidy could first have appeared as a failure to complete mitosis
at telophase, the stage where the doubled complement of chromosomes are usually
divided into two daughter cells. This would probably have spontaneously increased
the size of the eukaryotic unicell as wellthere is some correlation between cell and
genome sizes; large genomes need more space if they are to synthesize more proteins.32
Diploidy could also have been introduced through conjugation of two unicells with
homologous sets of chromosomes. In attempting normal mitosis the colinearity of the
DNA and histones in the homologous pairs could have been partially responsible for
synaptic pairing of the kind found in meiosis I prophase, although in most of the
familiar expressions of meiosis there is now a special protein apparatus that pulls them
together.
The next essential step in meiosis was to separate the pair of chromosomes in the
tetrad, without breaking apart at the centromeres as they do in mitosis. This modifi-
cation of the mitotic division restored the chromosomal complement of the daughter
cells to the original haploid condition. It must however be remembered that each
chromosome has already divided into sister chromatids held together at the
centromere. In primitive multicellular plants and animals the haploid condition
dominates the life cycle. For them, having diploid cells is no great necessity, except for
the brief period of chromosomal exchange involved in crossing over. That crucial
moment makes every offspring of the act of sexual association a potentially novel
emergent type. The conventional explanation for the dominance of diploidy in the
life cycles of higher terrestrial plants and animals is that it provides back up copies of
genes in case of damage from ultraviolet radiation in organisms directly exposed to the
sun. It also creates redundant genetic material for random natural experimentation
and the possibility of differentiating the sex chromosomes into dissimilar structures
like the X and Y in insects and mammals.
With sexual reproduction, the genetic variability that the eukaryotes lost when they
departed from the simple prokaryotic state was restored in a new form. Sexual
association of different individuals increased the potential for evolvability through
recombination of parental traits, gene duplication, and chromosomal mutation.
Chromosomal mutation provides for the position effects that Richard Goldschmidt
thought responsible for large phenotypic changes, i.e., hopeful monsters. That the
position of a gene, or smaller sequence of a DNA molecule is important in its function
108 Chapter 3
is no longer in doubt, especially through the work of Barbara McClintock on transpos-

able elements. Current research on the microtopography of DNA strands will
illuminate this further. In addition to chromosomal mutations, the duplication of
individual chromosomes, and of entire karyotypes contributes to evolution by
providing redundant DNA and proteins that can be differentiated to serve different
offices.
There is a last but not least detail regarding the evolutionary significance of
chromosomes, based on the work of Neil Todd (1970, 2000, 2001) and Robin Kolnicki
(1999, 2000). This has given rise to the karyotypic fission theory, brought to the fore by
Margulis and Sagan (2002). Todds original hypothesis was that another kind of
chromosome breakage was possible. All the chromosomes could simultaneously break
in two at the centromere-kinetochore, thereby doubling their total number. (The
centromere portion is DNA that is continuous with the rest of the chromosomal DNA;
the kinetochore portion is made of proteins that attach to the mitotic spindle.)
Mammals, the group that Todd surveyed, have disparate numbers of chromosomes.
Within one deer genus, Munjiacus, the diploid number of chromosomes varies from
three pairs to 23. Conventional wisdom gives the primitive mammal high numbers of
chromosomes that are then gradually reduced in number by chromosomal fusion
sorted, of course, by natural selection. How is it that within one genus the
chromosomal numbers are so widely different in the different species? Todds theory
of karyotype fission now proposes that the original mammals had seven pairs of
chromosomes. The molecular mechanism of fission involves an acceleration of the
reproduction of the centromere-kinetochore relative to the reproduction of the rest of
the chromosome. That acceleration can be the result of physicochemical changes that
affect the whole cell, so it happens in all of the chromosomes, making them more
likely to break when they attach to the mitotic spindle. Todd additionally posits that
fissioning events, which are unashamedly saltatory, were responsible for diversifica-
tion of the emergent types. This might have come from a greater degree of variability
that Margulis would subsume under her mix-match principle.
Multicellular Associations
Simple multicellularity emerged independently in several lines of evolution. Pre-
Cambrian algae were probably the first. Theoretically, the multicellular condition has
the advantage of being energetically more efficient for its cellular members, there
being a division of labor among them. Before there can be a division of labor, there
has to be a mitotic division that does not end with total uncoupling of the daughter
cells. A colonial protist such as Volvox survives without intimate links between its cells.
Cells with rigid walls can be held together by sticky exudates. But the cells of most
multicellular plants and animals have intimate links. Cell adhesion molecules allow
cells of the same type to recognize each other and stick together. The extracellular
portions of the class of molecules call integrins can attach, detach, and anchor cells
to each other, as well as to physical extracellular substrates. Since cell membranes are
fragile, the underlying fibrous cytoskeletons must be involved. Integrins provide part
of the cytoplasmic scaffolding that can order cellular biochemical pathways, as well as
inducing the formation of ultramicroscopic junctions that attach the cells to each
other, sometimes so tightly that water cannot penetrate between them. Other kinds of
junctions allow intercellular exchange of molecules.
Membrane receptor molecules initiate uptake of specific dissolved molecules or
particulate matter, or trigger cascades of hormonal responses in the cells. This allows
not only communication between adjacent cells but also between cells that are widely
separated in the organism. Some such cell surface molecules are found in primitive
unicells. Once they became involved in the formation of intimate, multicellular asso-
ciations, the repetitive differentiation of the genes coding for their synthesis became
an important feature of developmental evolution, and eventually generated the
emergence of the immune system in vertebrates.33
While sexual reproduction compensated for the loss of the ancestral genetic
flexibility of the prokaryotes, multicellularity conferred greater evolvability. It led to
the diversification of body plans, and to the progressive evolution of self-regulating
physiology. Thus, it contrasts with population adaptability based on the random
process of gene acquisition, possessed by primitive unicells. The progressive evolution
of the multicellular condition is a topic that I will come back to in chapter 5.
Meanwhile we will move on to the next major evolutionary performance involving
intraspecific associations.
Societies
If endosymbiosis is the alpha of associations, the omega is society. The entire spectrum
of associative evolution, from primitive symbioses through parasitism to human
societies, was regarded as grist to the mill of emergentism by the philosopher-entomol-
ogist William Mortimer Wheeler. However, like C. L. Morgan, Wheeler thought that
even such large emergences as life and mind were the cumulative and imperfect end
results of series of relatively small emergences.34 Herbert Spencer Jennings, who made
emergentism the Declaration of Independence for biological science (that is,
independent of natural selectionism and Laplacean reductionism), also cautioned
against forced comparisons of emergent systems operating at different phyletic levels:
If it is indeed in social organization that we find emergent evolution most manifestly at work, if
it is here that that which is new in principle most frequently and conspicuously appears, then we
shall be cautious in accepting the advice of even the King of the termites on our own social
problems; we shall use discretion and take his advice at most as suggestion toward experimenta-
tion. For any organism of society separated from others by steps in emergent evolution, the only
possible method for progress is by trial and error.35
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After 80 years this advice has not yet been heard by sociobiologists and evolutionary
psychologists who argue that gene-based heritable behavior patterns analogous to
those of insects and birds must also be present in humans.
This is not to say that useful comparisons between systems at different emergent
levels cannot be made. E. O. Wilson, successor to Wheeler in the study of social
insects, says he bases his synthesis of sociobiology on a quantitative holism that
involves the recognition and study of emergent properties.36 He infers, for example,
that human self-knowledge is shaped and constrained by emergent emotional
properties of the hypothalamus and limbic centers of the brain such as guilt, fear, love
and hatebut he believes that it was natural selection that made the hypothalamic
and limbic systems. In so doing, Wilson surrenders both sociobiology and
emergentism to ultra-Darwinism. He has also been accused of deterministic bias in the
analysis of human societies, and his natural heirs in evolutionary psychology go
even further in the same direction. Notwithstanding, sociobiology has a place as a
distinct subdiscipline of the general topic of evolution by association. Social interac-
tions produce emergent phenomena, which are by definition not driven (or
upwardly caused) by genes. Wilson has sought to identify such emergent
phenomena, and has compared them in insect societies with the operational system
of differentiated cells in a multicellular organism. While remembering Jenningss
epigraphic warning about taking the advice of the Termite King, such system
comparisons might also offer more focus on features of emergence common to other
evolutionary arenas.
Social insects have long been of interest for their apparent altruism or and
willingness to sacrifice their energy and their lives for the sake of the society. In many
cases, individuals are sterile, leaving reproduction to queens and drones. This has
given rise to the concept of the super-organism, with queens and males represent-
ing the sex cells and worker insects representing the somatic cells, selflessly sacrificing
themselves to the higher goal of reproduction. The idea was first mooted by William
Wheeler in 1911, elaborated by A. E. Emerson (1939), and R. W. Gerard (1942). But it
is now primarily associated with E. O. Wilson (1985). Interactions between social
insects certainly produce emergent behavior with properties not found at the
individual level.
Among the vertebrates, striking social behavior with emergent overtones is found in
the movements of schooling fish and flocking birds. But the most important social
associations for our own species have been family and tribal groups that culturally
evolved into modern societies. I will have more to say about societies later, but several
generalizations are appropriate at this point. One is that societies consist of groups
belonging to a single species. In some cases the members of the society are all
members of the same family, i.e., they are eusocial.
Now, having considered the various degrees of intimacy and mutualism that occur
in associations between organisms, what might we make of their ecological effects
during lifes history.
The Emergence of Ecosystems through Symbiogenesis
When Lynn Margulis suggests that the evolutionary importance of symbiosis has been
ignored by the Modern Synthesis, I agree, and I can think of several reasons. One is
that the Modern Synthesis subsumes anything it wants to salvage without bothering
to resolve contradictions in a truly synthetic manner, or to give credit where due. In
the case of symbioses, the Modern Synthesis simply argues that natural selection
builds them, approves them or eliminates them. A tacit reason for the Modern
Synthesis to underplay symbiosis is that evolutionary symbiogenesis really belongs
with saltatory emergentism. Margulis has a global view of the importance of symbiosis
in the life of Earth, and her treatment of the most significant oneeukaryotic
endosymbiosishas been exhaustive. Yet her thesis has underemphasized the
historical impact of symbiogenesis in the foundation of all of the major ecosystems.
Thiobios
This is an ancient trophic system established by the archaean prokaryotes that used
volcanic sulfur as a primary source of energy. Once animals diversified through the dif-
ferentiation of multicellular forms, the thiobios could be expanded through
bacterial-animal associations that exist in some bivalves, gastropods, annelids,
pogonophores, and echinoderms. Hosts created ideal physiological environments for
such symbionts, and in return they received simple organic products synthesized by
their symbionts, using the energy of sulfur. The bacteria may be found inside host
cells, or in blood spaces, loosely associated as epiflora on the outer surface of the host
or in aerated chambers formed in organic sediments by infaunal metazoans. Several
different species of sulfur-oxidizing bacteria have been discovered in such relation-
ships, which are now well known in several families of bivalve mollusks.
Although Tom Fenchel and Rupert Riedl had recognized the significance of the
thiobios in 1970, the reaction of benthic biologists was indifferent until the flurry of
research began on marine thermal rift communities. The thiobios is at its most
conspicuous in deep water volcanic thermal vents that supply a mineral source of
sulfide. Conspicuous is not meant literally, since the first examples were found by
submersibles at a lightless depth of three kilometers in the Galapagos Rift only two
decades ago. There, rich communities of the huge symbiotic pogonophore tube worm
Riftia have grown up along with vent clams and mussels, supporting a tertiary trophic
level of gastropods, crustaceans, and fish. These are oases of energy in an otherwise
barren, benthic wasteland. The thiobios also exists in a more diffuse form on
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continental shelves where there are organic sinks with high sulfide levels produced by
bacterial decomposition.
Marine Photosynthetic Ecosystems

Although the thiobios is an ancient and interesting ecosystem, photosynthetic
systems dependent on the energy of light have a much more universal distribution.
The largest biomasses of the marine food chain depend on the symbiosis between
chloroplasts and plant cells, especially phytoplankton. Moreover, the impact of pho-
tosynthesis on the oxygenation of the oceans and the atmosphere was one of the
largest ecological and evolutionary impacts in the history of Earth.
Most benthic ecosystems depend upon light as their primary energy source.
However, in the tropics, while light is not limiting, soluble plant nutrients such as
nitrogen compounds and phosphates are. Consequently the tropical benthos is
relatively barren, with the exception of coral reefs. The modern coral reef, now
ubiquitous throughout warm seas, has a complex topography, with a richly diverse
community of plants and animals. All this is founded upon a symbiosis between
dinoflagellate zooxanthellae and the reef-building coral cnidarians. Again the host
provides cellular living space and metabolic nutrients such as ammonia, carbon
dioxide, and phosphates that the algae can photosynthetically convert to carbohy-
drates, amino acids, fats and nucleic acids. Some of these are returned to the host. In
the mineral nutrient-deficient coral reef environment, the photosynthetic zooxanthel-
lae acquire nitrogen and phosphorus from the animal food of the corals. The food
consists of small invertebrates and fish that are captured by the nematocysts
(stinging cells). Nematocysts may be symbionts that first evolved as independent
unicellular microsporidians.37
Coral zooxanthellae have been passed on as symbionts for other animals, such as
sea slugs that feed on coral.38 Tridacnidaethe family of giant clams that live in the
reefsalso feed on zooxanthellae and particulate debris released from heat-stressed
corals as phytoplankton, though they are resistant to digestion. Symbiogenesis
between dinoflagellates and the clams has resulted in a drastic allometric shift in the
clams shell and soft anatomy, providing a greater area of tissue to house the
symbionts where light is most available. Photosynthetic symbioses occur sporadically
in other kinds of marine animals such as flatworms and polychetes, but only in the
coral reef do they provide the foundation of an ecosystem.
Terrestrial Plant-Fungus Ecosystems

It wasnt until plants spread to land that their functional-morphological complexity
began to emerge. The littoral was already occupied by biofilms and mats of blue-green
prokaryotes, simple algae, bacteria, protozoa, and perhaps fungi. The first truly
terrestrial emergence was made by the kind of association of algae and fungi found in
lichens. These constitute a polyphyletic group, meaning that their members emerged
independently numerous times. A similar, but even looser, association persists in the
great majority of the higher land plants.39 Familiar woodland mushrooms are the
fruiting bodies of symbiotic basidiomycetes that invest tree roots as mycorrhizae,
enabling nutrient exchange between partners. Once their foothold on land was
stabilized by symbiotic fungi, the plants were at liberty to experiment with morpho-
genesis and reproduction.
In Symbiotic Interactions (1994), Angela Douglas argues that mycorrhizal symbioses
must have been established at the points of origin of the major groups.40 In other
words, they were pivotal emergences of land plant evolution. In some instances,
mycorrhizal symbioses involve a third party, such as squirrels that dig for the fruiting
bodies of truffles, and help spread their spores by breaking them open in the safety of
a tree. From their germination new mycorrhizal strands invest new trees that the
squirrels will eventually climb to enjoy the fruits of their labors and help them
propagate once again.41
Cellulolytic Symbioses
Do humans who drink milk and eat meat know that the major resource for these
habits depend on a symbiosis between cellulolytic micro-organisms and their cattle
hosts? Perhaps more than 400 million years ago, in the terrestrial environment, a new
food pyramid emerged from a symbiosis that utilized cellulose. A generative condition
of much of plant evolution was the possession by some algae of cellulose walls. These
helped them survive first of all in fresh water, by resisting excessive water intake.
Then, when plants invaded land, their rigid cellulose cell walls and vessels, supple-
mented later with woody fibers, provided the framework for the vertical architecture
of bushes and trees. The first animals that arrived on land, probably flatworms,
oligochete worms, gastropods, crustaceans, and proto-insects, found a primary
resource that was partly inaccessible. Little cellulose food had been available to their
marine ancestors, and although some could digest simple cellulose, most of them had
lost the appropriate enzymes. Fortunately for the incipient terrestrial food pyramid,
this is not so for soil fungi, bacteria and protozoa that were to become symbionts.
Herbivorous invaders of the land foraged in decaying plant material; primarily because
plant cover and vegetable mold provided some protection from the sun and from
desiccation. In addition, the breakdown products of decomposing plants are more
accessible to simple digestive systems than native cellulose, and the fungal mycelia
that run through the decaying plants are also digestible. The lifestyle and simple
morphology of the land isopod crustaceans that are variously called wood-lice,
slaters, or pill-bugs are probably very similar to those of the primitive crustaceans
that first made landfall.
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Some of the bacteria, with their group adaptability in responding to novel and harsh
environments, were or became resistant to digestion, and established themselves as
gut symbionts in the invertebrate pioneers. Some protists did the same, including one
of the most symbiotically complex creatures, Myxotricha paradoxa, which is found in a
primitive Australian termite. The protist host cell has the usual eukaryotic mitochon-
dria and undulipods. Two kinds of spirochete bacteria attach to the outer coat at
specific sites, one type amounting to about half a million cells per host cell, organized
to provide a coordinated locomotion for the whole organism.42 With such symbionts,
crustaceans, insects and slugs and snails could get much more out of the plants they
ate, and these new herbivores spread rapidly. From this secondary terrestrial trophic
base, a third level of carnivores was extended. Biochemically this required no great
novelty since they already had the enzymes needed for digesting animal food. It was
only a matter of cranking up the proportions of peptidases to make the digestion of
animal protein more effective. Specialized predatory behavior and raptorial
mouthparts were secondary.
Nitrogen-Fixing Symbiosis
Nitrogen-fixing symbiosis is largely confined to plants, many of which live in environ-
ments with few available mineral nitrogen compounds. Here, some plants, such as
Venus flytraps, sundew, pitcher plants, and butterwort, are insectivorous, actually
digesting animal protein to acquire usable nitrogen. Many, including peas, beans,
vetches, alders, and other woody flowering plants, have symbiotic bacteria that fix
atmospheric nitrogen to make ammonia. When the germinating seeds pick up the
appropriate soil bacteria. (Rhizobium and its relatives in the case of the legumes) the
young host plant grows nodules that house them. Although the symbiosis is energet-
ically expensive for the host, it has a large ecological impact by contributing to the
invasion of barren wastelands and providing for a subsequent succession of non-
symbiotic plants. The symbiosis is probably key to the emergence and diversification
of the common and pea and bean family Viciidae.
Now that some of the major impacts that symbiogenesis has had on evolutionary
history have been outlined, some philosophical aspects of association can now be
explored, beginning with another aphorism of Aristotle.
The Whole Is Greater Than the Sum of Its Parts
The many routes to greater complexity, and to new wholes that are greater than the
sums of their parts, will be illustrated in this chapter and in the next two chapters. The
symbiogeneses that occurred during cellular evolution were among the earliest and
most striking examples of the principle. That an emergent association has the
potential to be a whole that is greater than the sum of its parts is virtually a truism.
But it is unfortunate that such a concept should pass into triteness without analysis,
since it is not only relevant to symbiosis, but also central to the development of
emergentism. Reductionists have traditionally argued that ignorance of the whole is
mere ignorance of some of the parts, and that the emergent properties of a whole can
be ignored if one knows all the features of the parts. John Stuart Mill pointed out more
than a century ago that the holistic properties of water cannot be predicted from a
mere knowledge of the characteristics of oxygen and hydrogen. But, argue the reduc-
tionists, it is so simple: water and its properties are merely the qualities of hydrogen
and oxygen in combination with each other!
The emergent quality of water is not that easily explained away by simplistic holism,
any more than reductionism. The emergent properties of water or any other whole are
difficult to predict from a knowledge of the nature of the components. It makes it
easier to describe them by working back from the known combining features.
Although unpredictable combinatory uniqueness is a mark of some emergent
properties, evolutionists of all stripes have to operate by hindsight, because the events
under investigation have already happened. And generating concepts of future com-
plexities is not in the usual repertoire. Taking care not to smuggle our existing
knowledge of the outcome into the exercise, it might be possible to post-predict, i.e., to
estimate if known complexities would have been predictable from a knowledge of the
historical conditions that generated them. But it would be hard to imagine the
possibility of mutualistic, symbiotic wholes in a universe where they had never
occurred. Even when the evidence from looser associations such as lichens and coral
was staring us in the face, biologists, including myself, initially resisted the radical
notion that mitochondria were symbiotic. But in our enlightened state we finally see
that this endosymbiosis beautifully illustrates the principles of complexification by
association.
Complexification by Association
It is easy to see the mutualistic potential when a protomitochondrial, independent
organism takes residence in an anaerobic prokaryote. Simply tabulate the biochemical
characteristics of the mitochondrial symbiont and the rest of the eukaryotic cell,
ignoring, for the time being, the fact that genes and functions were exchanged and
some may have regressed over the course of time. Among other things the cellular
cytoplasm uses simple carbohydrates, in the absence of oxygen, to make a small
amount of the high-energy compound adenosine triphosphate (ATP). The mitochon-
drion removes from the cell ammonia and ammonium ions, toxic compounds that
results from amino acid metabolism, and turns them into other amino acids, or
initiates synthesis of urea and uric acid (which are less toxic than ammonia). This
perhaps was part of a primitive ability of the promitochondrion to use inorganic
sources of nitrogen for the construction of amino acids, proteins, nucleotides, DNA,
116 Chapter 3
and RNA. The mitochondrion also removes oxygen from the cell to produce copious
ATP. Remembering that oxygen was a toxic compound in the ancient anaerobic
biosphere we can see that the symbiosis turns detrimental, or negative qualities into
positive ones. Even by simple arithmetic, the whole, in concert, is greater than the
sum of the parts.
Symbiogenesis thus provides a way of emerging to new wholes that are greater than
the sum of their constituent wholes. The condition of new wholeness that emerges
from symbiogenesis is largely due to complementarity of the biochemical, physiolog-
ical, and behavioral functions of the pre-symbiotic individuals. Margulis (1981) and
Douglas (1994) provide long lists of emergent metabolic properties of symbioplexes.
Having looked at the spectrum of associations that range from the most intimate
and mutualistic to the loose and lopsided, and having discussed generalities about
emergent wholes, we return to the chronology of their evolution. Where to begin?
The first major biological emergence was that of life itself, and the nature of the first
cells that appeared. This is a matter of molecular association, which will be considered
in the next chapter. At this point it is enough to note that the first protobionts were
simple systems that did not have the full range of genetic faculties that we associate
with modern bacteria. They had to reproduce fast enough to keep up with wear and
tear, aided by a catalytic capacity to energize essential molecules for polymer
synthesis. Their reproduction also had to be faithful enough to ensure survival of
functional phenotypes. In the absence of any defensive digestive or immune systems,
protobionts with simple phospholipoprotein membranes could freely coalesce and
become more complex systems with emergent properties arising from the complemen-
tarity of previously independent features. Mere compatibility could simply have been
enough to ensure their persistence. However, the greater quality is adaptability.
Eukaryotic Emergence
The emergence of eukaryotes through endosymbiosis between primitive prokaryotes
was the most important complexifying saltation in the evolutionary history of living
organisms. How it occurred is still a matter of speculation, since the most appealing
mechanismphagocytosisis not employed by modern bacteria. Margulis originally
suggested that predatory heterotrophic bacteria were prime candidates as endosym-
bionts.43 These normally lyse and enter the prey cells, seal the breach, and then digest
their surroundings at their leisure. If the assault was limited to lysis, entry and
resealing, with subsequent destruction of the prey inhibited, sharing of resources
could have ensued. But this explanation creates the problem of how the double
membranes of mitochondria arose. Therefore phagocytosis, which temporarily
combines the membranes of both predator and prey remained appealing.
One popular current idea suggests that enlarged Thermoplasma-like Archaea were the
original kind of host cell.44 This is partly based on the fact that Thermoplasma is more
accessible since it lacks a rigid cell wall, and the discovery of Archaea genes in the
eukaryote nucleus.45 Archaea have both the interior endomembranes that could
have given rise to nuclei and endoplasmic reticula, and a cytoplasmic skeleton that
could have provided the contractile threads necessary for phagocytosis.46 The
archaean Archeoglobus has many protobacterial genes, relicts of transitory transgenetic
brushes with other bacteria over the course of time.47
Margulis and Sagan (2002) have put an interesting twist to the idea of an archaean
Thermoplasma-like host by combining it with a spirochete. It not only gave the
symbiosis a metabolic complementarity between sulfide production and oxidation,
it also added undulipod motility. They postulate that the original host was a heat-
resistant archebacterium whose metabolism used the energy of sulfur, with hydrogen
sulfide as an end product. A spirochete that used the sulfide as an energy source
became endosymbiotic with the archaebacterium. Not only did they pool their
metabolic resources, the sulfide scrubbed free oxygen, which was beginning to
appear in the environment at the time. Thus, the spirochete which was completely
vulnerable to the toxic oxygen was protected.48 The symbioplex could now seek
the most mutually beneficial gradients of sulfur and its compounds, acidity, and
oxygen.
A corollary of the model also suggests how the nucleus arose. To do so it draws upon
the nature of the karyomastigont, i.e., the complex consisting of nucleus, the cilium
(or undulipod) and the fibrous protein connection between the two. Margulis and
Sagan call it an emergent structure of the original symbiosis.49 Imagine that the part
of spirochete symbiont that intruded into the host retained its surrounding cell
membrane, containing its genophore. The undulipod was left at the surface of the host
where it continued to be a locomotory organ. How the genophores of the archean and
spirochete coalesced within the protonucleus is unknown, but exchanges of the
smaller gene-containing plasmids between bacteria is common. And there are
variations on the theme, arising from differential growth rates of host and symbiont,
giving rise to some cells with multiple karyomastigonts, some with multiple
undulipods, some with multiple nuclei and some without nuclei. All these variations
still exist in nature. And once the genophores became chromosomes there was a kary-
omastigont fibrous protein system and a set of centrosomes ready to participate in
mitosis and meiosis. The hypothesis is both parsimonious and predictive, and
illustrates how a single emergence can have so many immediately beneficial properties
and great evolutionary experimental potential.
The later acquisition of protomitochondria would have compounded the oxygen-
scrubbing function already present in the original host. Another interpretation of
the mutualistic benefits of the endosymbiosis involving mitochondria, is that it
could have been based on hydrogen production instead of respiratory exchanges and
detoxification.50 Some -proteobacteria, of the kind generally agreed upon as the best
118 Chapter 3
protomitochondrial candidate, excrete hydrogen and carbon dioxide as metabolic

byproducts of the oxidation of organic molecules. (Mitochondria now retain the
hydrogen ions for the production of ATP.) Also, some Archaea depend upon hydrogen
and carbon dioxide as the only source of energy and carbon for their metabolism. The
two could thus combine in a state of instant mutualism. At that point the mitochon-
dria need not have detoxified oxygen. But they were poised to use oxygen as a
hydrogen acceptor, once phagocytosis had provided a more satisfactory alternative
source of energy for both symbiont and host.
This degree of functional complexity was only surpassed when another endosym-
biosis gave chloroplasts to some of the eukaryotes. Prokaryotes that became
chloroplasts were already symbioplexes with complementary photosystems derived
from two previously independent prokaryotes.51 The endosymbiotic hierarchy may
have been further compounded: traces of nuclear material in some algal chloroplasts
suggest that after photosynthesizing unicellular eukaryotes had been established,
some of them, in turn, became symbionts in other algae. Karl Niklas notes that
something old, something new, something borrowed, something blue takes on
special significance for algal marriages.52
Photosynthesis originated before the emergence of eukaryotic algae, but it is not
clear how quickly nor to what degree it oxygenated the old reducing environment.
While there would have been temporary oxygenated pockets, there was a large,
inorganic sink that required filling before free oxygen could spill over. That surplus
would initially be used up by the oxidation of organic debris from dead bacteria. But
if organic remains were sequestered as fossil material the balance would shift to the
side of free oxygen. Algae were the first organisms to tilt the proportions enough to
finally ensure the general accumulation of free oxygen in the water and in the
atmosphere. Thus, they had double emergent properties: their own physiological
qualities and their ability to convert the anaerobic environment to an oxygenated
one. This environmental contingency would have been catastrophic for many obligate
anaerobic organisms, clearing the bench for new experimental forms. Their deaths
would have initially wobbled the supply of free oxygen. But eventually the
oxygenation of the biosphere was to make causal waves that would surge through
time, leading to the evolution of air-breathing animals. Their high-oxygen-dependent
metabolic rates would eventually support a homeothermic physiology, and the
emergence of sophisticated nervous systems and mind.
The notion that chloroplasts were once independent, free-living micro-organisms
had been suggested by W. Pfeffer in 1881, and elaborated by A. F. W. Schimper in 1885.
In the same decade, K. Altmann had speculated that mitochondria had similar
origins.53 But considerable resistance to these historical ideas persisted until Lynn
Margulis established the theory of serial endosymbiosis in 1970. Even then it took a
decade of persuasion, and the unearthing of new molecular evidence, to supplant the
direct filiation theory. That alternative theory had postulated that organelles were
secondarily derived from the outer cell membranes by a slow and complex process of
invagination and involutionthus explaining why mitochondria and chloroplasts
had double sets of membranes. Although the hypothesis that the organelles acquired
the extra set of membranes when they took up residence in the host cell is more par-
simonious that the direct filiation theory, it was the latter that lent itself better to
Darwinistic gradualism.
Some complained that endosymbiosis was a cheap explanation: The endosymbio-
sis hypothesis is retrogressive in the sense that it avoids the difficult thought necessary
to understand how mitochondria and chloroplasts have evolved as a series of small
evolutionary steps.54 The critics then compounded their polemic by accusing the
endosymbiosis hypothesis of playing into the hands of the bogeyman of special
creation. But the selectionists real worry was that endosymbiosis is a supreme
example of saltation: a prokaryote can only enter the association as a whole organism,
and the new whole is immediately a doubly complex structure with an array of
emergent qualities. As Darwin feared, if the monster is successful at birth, with
intrinsic features responsible for its survival and reproduction, natural selection has no
part in its construction, except in the adjustment of a stable internal equilibrium.
Apart from the debatable origin of organelle membranes, and the parsimonious
appeal of endosymbiosis, it was already known that organelles have their own DNA,
and independent reproduction within the cell. Then, DNA sequencing evidence began
to show that chloroplasts and mitochondria are much closer to extant, independent
prokaryotes in their DNA structure than they are to the chromosomal DNA of the
eukaryotes that house them.55 Their functional morphology is also more bacterial than
eukaryotic. Organelle DNA is organized like bacterial genophores, not in protein-
associated chromosomes. They undergo binary fission like bacteria. The translation
mechanism and ribosomes are typically bacterial, and their outer membranes have
biochemical characteristics similar to bacteria.
The new eukaryotes with mitochondrial and plasmid symbionts largely abandoned
prokaryotic transformation, the ability to absorb naked genes, and plasmid transfer by
conjugation. Nevertheless, transposable elements have persisted all the way to
humans. Viruses have been variously described as pathogenic, neutral, or a source of
variation. Viral transduction remains a dark horse, detrimental in some cases, yet a
potential universal source of molecular saltation. In addition to retaining these
features of saltatory evolution, the eukaryotes were the first to acquire true sexual
reproduction, and along with it the potential for chromosomal and genic mixing, to
gain a wider spectrum of variation within individuals and populations. The new cells
were more adaptable as individuals than their prokaryotic ancestors.
Primitive eukaryotes sorted themselves out into the forerunners of the major lines
of evolution: the Protoctista (or Protista, as they used to be called), single-celled and
120 Chapter 3
multicellular, some photosynthetic and others not; the photosynthetic and multicel-
lular Plantae; the unicellular and multicellular, non-photosynthetic Fungi; and the
multicellular Animalia. Along with the prokaryotic Monera they make up Whittakers
five kingdoms of living organisms.56 Some of these major groups are polyphyletic, and
the Protoctista were variously ancestral to the plants, fungi and animals. However, for
the sake of simplicity, we will accept the five kingdoms as they stand, albeit arising
from the two founding domains: Archaea and Bacteria. The primary concern for the
moment is how they all entered into associations that are among the most significant
emergences of evolutionary history.
Symbiogenesis
Can general principles be inferred about the generative conditions for symbioses?
There are two major requirements: first the participants for potential symbioses must
be present together, and in sufficient quantities for natural experiments to be possible.
A common affinity for the same environmental locus is obviously significant.
Common nutritional needs, predation, infection, or parasitism can get two different
types of organism into intimate, non-mutualistic proximity. But for them to become
symbiotic, defensive mechanisms of the potential hosts, and detrimental parasitic or
predatory effects by the potential symbionts must be absent, repressed, or removed.
Since these are likely to be rare occurrences, the necessity for large numbers of
potential participants is all the greater.
Before the symbiogenesis of the eukaryotic condition, congregation of the future
partners at an environmental interface must have been a generative prerequisite. If, for
example, endosymbiosis involved a host cell with anaerobic or weakly aerobic
metabolism, and a proto-mitochondrion with aerobic metabolism, they may have met
at a redox layer with oxygenated water on one side and anoxic water on the other. In
the oxygenated water there would also have been the proto-chloroplasts responsible
for the oxygen output in the first place, and already inured to oxygen toxicity. As
much as being in the right place at the right time, the crucial rallying cry for potential
associates in this symbiosis is to be in the same place at the same time. That several
different unicellular types did so allowed their consequent mixing and matching. That
the right place did not come into existence for a billion years or so after the origin of
life helps to explain the long delay in eukaryote emergence. It also emphasizes that
however plastic the genetics and biochemistry of prokaryotes, their evolutionary
potential is feeble in comparison with sexually reproducing, multicellular organisms.
The mix-and-matchability of their cells was involved in the evolution of new organs,
but diminished as those became specialized. All was not lost, however, since migratory
organizing cells could create new combinations.
One feature of symbiostasis, control of symbiont numbers by the host, may provide
for the establishment of new symbioses. Excess numbers of Symbiodinium, the
symbiont of corals, which may become toxic at high temperatures, are expelled by the
host. While swimming on tides flooding over a heat-shocked coral reef I have several
times experienced a zone of warm green water containing free coral dinoflagellates.
Global warming now appears to have intensified the effect to the point of destroying
some reefs.57 Normally these regions in high summer always contain numerous
symbionts available for setting up shop in new hosts, as well as fodder for filter feeders
that would otherwise find the tropical sea rather barren of food.58 This is how the
ancestors of giant clams obtained their symbionts.
In thermal vent regions of the ocean where volcanic sulfide escapes into oxygenated
water there are so many free-living sulfur-oxidizing bacteria that they coat every
surface, including the exposed gills of filter feeders that collect them as food. This mul-
titudinous proximity, and high probability of ingestion by larvae, must have been
important in establishing thiobiotic endosymbioses. All of the bivalves in the vent
regions are symbiotic. In contrast, few bivalve types, and even fewer of the other inver-
tebrates elsewhere in the ocean, have the symbiosis. Despite all of the other potential
advantages and opportunities, most bivalves close their shells tight in the presence of
sulfide, or die if they cannot somehow avoid it.59 Two ancillary emergent features for
this association are the abandonment of the quintessential bivalve character of
clamming up, and maybe having the ability to tolerate or detoxify sulfide.
Like all other emergences, the sulfide-oxidizing symbiosis had to meet several
generative conditions that were long in accumulating. However, the symbiogenesis
itself is both saltatory and mutualistic, since the first bacterial cells could immediately
begin to exchange nutrients and combine resources with the host. In the sea, free-
living sulfur-oxidizing bacteria are close to the redox interface between oxygenated
and deoxygenated environments, and this fluctuates according to the production of
sulfide and the turbulence of the water. The clam host offers a saltatory environmen-
tal improvement for its bacteria by regulating that redox interface and ensuring
continuity of metabolic needs.
It should now be clear that one of the most universal processes of symbiosis among
primitive microorganisms, and then between them and animal hosts, is ingestion. For
the process to succeed, the microorganisms must reproduce faster than they are
digested, or become indigestible. This route for the establishment of symbionts has
been established time and again, and it still happens in the case of horizontal trans-
mission, where the symbionts are not passed to the next generation via the egg, but
are recruited from the external environment.
Fungal-algal symbioses could have been established simply by congregating at
marine or freshwater shorelines. They must also have mingled in multi-organismal
strands in shallow ponds subject to desiccation. As for cellulolytic symbioses, the
122 Chapter 3
symbionts were in the beginning universally distributed among decomposing plant

material, and regularly ingested. A minimal resistance to digestion was needed to
allow it to set up accommodations in the hosts gutespecially if the main chamber
where it could operate was in advance of the normal stomach, as in ruminants. The
novel proto-symbionts were then recycled through the feces of the host to be spread
through the population of animalsas much a Lamarckian as a Darwinian
development, since all of the animals ingesting the bacterial spores with their
vegetable diet were simultaneously affected. Later there came a number of develop-
mental experiments in guts that could accommodate the symbionts efficiently.
At the most complex end of the spectrum of association are familial and social
groups, whose success also requires the participants to be in the same place at the right
time, to exchange not only nutritive and emotional energy, and not only information,
but wisdom.
Epigenetic Effects of Symbioses
Major complexifications during the early history of life were due to the establishment
of symbioses in themselves. The subsequent major phase of complexification involved
cell multiplication and differentiation in multicellular organisms. Symbionts also
contribute to this later phase through epigenetic effects on their hosts that influence
gene expression or cell division. (Epigenetics refers to the normal and evolutionary
processes of development.) The intestinal bacteriome that is found in many fluid
feeding insects consists of large cells whose polyploid condition echoes that of the
root nodule cells of leguminous plants. Flavinoids from the young host plants
stimulate their Rhizobium symbionts to produce nod factors, glucosamines that in
turn stimulate the production of nodulin in the plant. This stimulates growth of the
nodules that house the symbionts, as well as membrane formation in the intracellular
symbiosome, which is distinct from normal cell membrane.60
Thallus formation by the fungal component of lichens is stimulated by the
symbiotic algae. Another example of an interspecific though not quite symbiotic
epigenetic effect is the curious morphogenesis of sea lettuce genera, Ulva and
Monostroma, which have presumably had characteristic lettuce-leaf thalli for most of
their evolutionary history. Yet, this development requires the presence of epigeneti-
cally stimulating, free-living bacteria. In axenic (bacteria-free) culture the sea lettuces
develop as masses of threads instead of their usual single broad thalli.61 A similar but
more intimate epigenetic influence comes from symbiotic bacteria in Ardisia, a
tropical flowering plant with fluted leaves. The leaf form and the successful growth
and reproduction of the plant depend on the presence of the intercellular bacteria that
are passed vertically in seeds. Diversification of the genus and its relatives may largely
be the result of symbiosis with this and other similar bacteria.62
Not only plants are profoundly affected by the epigenetic effects of symbionts.
Intestinal bacteria influence the functional development of the mouse gut.63 Multiple
mechanisms, including digestive enzyme activation, immunity, mucosal defense,
nutrient absorption, and normal postnatal gut development, all have some
dependence on the presence of the commensal bacterium Bacteroides thetaiotamicron.
How far back in the evolutionary history of symbiosis between bacteria and
eumetazoans did such epigenetic influences originate? They are certainly not gene-
determined by the host, nor even innate in the conventional interpretation of the
term. Influencing the nature of their accommodations through epigenesis may be a
common attribute of symbionts. Could the profound allometric expansion of the
siphons of giant clams, where photosynthetic symbionts are housed, have been
triggered by the dinoflagellates? Could the proliferation of bacteriocytes or even pae-
domorphosis in sulfur-oxidizing bivalves have been stimulated by their symbiotic
bacteria, or by high tissue levels of sulfur compounds?
Symbiostasis
As Lynn Margulis says, symbiogenesis is like a flash of evolutionary lightning.

Dazzling as that is, a lot of the foot-slogging needed to advance our knowledge of such
emergences involves the establishment of the dynamic stability between the
associated participants. In some cases, such as endosymbiosis, stasis is a desirable
consequence of emergence. While symbiogenic experiments are saltatory, they are
crude at the time of origin, and mutually beneficial adjustments are made by both
parties as time goes by. Evolution progressed through epigenetic emergences built
upon multicellularity that had emerged from endosymbiotic unicells, and founda-
tional symbiostases were established at each level. Members of associations like
endosymbiosis and differentiated multicellularity became so mutually attuned that
they have hardly ever been undone. However, when associations are initiated, even if
they are immediately mutualistic, the emergent wholes may lack the special
competitive qualities of their formerly independent constituents, and may lack a cohe-
siveness that guarantees their continued co-existence. One disadvantage to symbiosis
is that the partners become hostage to each others fortune.
An important aspect of symbiostasis is limitation by the host of the population of
unicellular symbionts. Commonly, the reproductive rate of the symbiont is lower in
the host than that of similar free-living micro-organisms, and the control mechanism
is usually assumed to be the limitation of symbiont nutrients. Giant clams farm their
symbionts to some extent, their amebocytes culling and digesting the senescent cells,
and delivering them to the giant kidneys of the clam for final processing.64 Surplus
cells are also extruded through the digestive system, whence they can enter juvenile
hosts. In sulfur-oxidizing symbioses, the hosts probably lyse aging bacteriocytes and
124 Chapter 3
the symbionts that they contain. Aphids somehow control the rate of division of their
bacterial symbionts, although they increase in size. And the bacteria of mature aphids
are lysed along with the mycetocyte cells that contain them.65 Other adjustments, in
the first eukaryotes for example, included the surrender by the mitochondria of most
of their protein synthesizing capacity to the host nucleus. Nuclear genes became
organized into exon subunits that could be combined in a variety of ways, and after
chromosomes emerged they were mixed and matched to make up linkage groups that
sustained interactive gene coordination, and hence organismic wholeness.
In some instances, symbioses have resulted in marked changes in the physiology
and morphology of the hosts. After they got symbiotic dinoflagellates, giant clams
stood on their heads and expanded their posteriors into massive siphonal pastures for
their symbionts. A correlated growth of giant kidneys dealt with the new metabolism.
Bivalves with sulfur-oxidizing symbionts sometimes underwent paedomorphosis or
found other ways of increasing the gill volume to house their bacteria. Radical changes
in gut anatomy followed the establishment of cellulose-digesting bacteria in terrestrial
herbivores. Nitrogen-fixing bacteria established epigenetic feedback pathways that
resulted in root-nodule formation. I have hinted that the symbionts themselves are
epigenetic catalysts of physiological and anatomical change in animals. And all
manner of anatomical arrangements have been made by terrestrial plants that
optimize the photosynthesis of their chloroplasts. So after the establishment of the
symbiosis, in addition to the minor changes and adjustments that contributed to sym-
biostasis, there have been emergent, epigenetic processes of allometry, and life cycle
alteration that will require further examination in chapter 5.
At the beginning of this chapter I proposed to survey symbioses, sex relationships,
multicellular associations, and societies. Symbiosis, despite its many manifestations,
forms a coherent topic, which demonstrates how very dissimilar types can interact for
the benefit of the whole. But, in reserving the major discussion of cellular interactions
for chapter 5, I have left a weak link between symbioses and societies. In the following
section I reinforce that link with a discussion of how some authors have compared
cellular associations with animal societies. I also assess the heuristic qualities of such
comparisons.
Societies, Cells, and System Reductions
First, I wish to introduce the useful vocabulary of E. O. Wilsons Sociobiology. I do not

intend this to be a general preamble to, or endorsement of, sociobiology as he
conceived of it, although the topic has a legitimate place in general zoology. Second,
I evaluate two examples of system reductions that compare societies to cellular associ-
ations. System reduction, which is derived from general systems theory, is a method
for understanding a complex system by analyzing a simple system that is sufficiently
similar to allow legitimate inferences to be made.
Wilson uses the traditional definition of society: a cooperating group of

conspecific organisms.66 An aggregation is a group with minimal communication
and no organization, brought together by extrinsic conditions to enjoy some mutual
benefit such as keeping warm in winter. A colony is a highly integrated group with
specialized members, and Wilson applies the term to associations such as hydroid
cnidarians with differentiated zooids, as well as social insects. These associations are
eusocial, meaning that the individual members are genetically identical or highly
similar because they are siblings. The original sense implied by a human colony, a
transplantation that has a similar social structure to a parental society, is excluded.
Group is a flexible term indicating a subset of a population whose members interact
more strongly than they do with other members of the population.
Wilson limits symbiosis to interactions between different species. Social symbiosis
is used for social animals that associate with different species, such as ants that have
domesticated aphids and scale insects that supply them with honeydew. These rela-
tionships can be divided up into social mutualisms, commensalisms, and parasitisms,
which are self-explanatory. Wilson defines the following qualities of societies. Since he
subsequently compared the insect society superorganism to an organism composed
of cells, I add my own comments on cellular and social parallels in brackets.
Cohesivenessthe physical proximity of members of the group that enhances commu-

nication, distribution of food and defense. [The comparison with multicellular
systems is self-evident.]
Connectednessin the absence of unpatterned connectedness a communication signal

is passed to all of the nearby members of the group, an alarm call in a flock of birds,
for example, without discrimination even as to species. If the group has a hierarchical
structure, signals can be confined to particular subgroupsthe bellow of a rutting stag
to other mature males, for example. [Within an organism a widely broadcast
hormonal signal is only picked up by cells that have the appropriate specific
recognition sites. Neurons have hard-wired connectedness, plus a phenotypic ability
to experiment with dendritic connections.]
Permeabilitythe degree of how open groups are to intermingling. Some social groups
never accept newcomers, others accept them freely. [Prokaryotes are permeable to the
genes of other individuals, not necessarily of the same type, but, by and large, perme-
ability at the organism level through exchange of cells is confined to sexual
reproduction and symbiogenesis. It could be argued that changes in the movement of
organizer cells in development that contribute to evolutionary change might be
included in this category. Permeability increases gene flow, but in social groups it
tends to destabilize their interpersonal structure.]
126 Chapter 3
Compartmentalizationthe organized complexity of both societies and organisms

depends upon the degree of independence of the subgroups. Under attack, wildebeest
leave their calves to be defended by the mother alone. Wilson contrasts them with
zebra, which form defensive family units with the stallion taking a prominent
protective role. He also cites ants that build semi-independent nests that exchange
individuals with each other and have the potential to become mother nests if the
original maternal site is destroyed. [Cellular compartmentalization of this kind is weak
in lower animals and plants that can regenerate whole organisms from damaged parts.
In higher animals artificial cloning is possible, but the original organism cannot lose
essential compartments or organs without losing its integrity or being adversely
diminished. Indeed, compartmentalization is part of a general trend of progressive
evolution, contributing to the emergence of a sophisticated physiological
homeostasis, and ultimately mind.]
Differentiationof roles in the case of societiesof cells in organisms. Ontogenic dif-

ferentiation in societies of ants and marine animal colonies is a function of population
density. [This is true to a limited degree in cell specialization in multicellular
organisms as well, although it is also linked to evolutionary status. Human societies
do not differentiate like ants, but there is division of labor and specialization of some
functions that has equivalent social advantage.]
Integrationa complex social system implies mutually beneficial integration of

behavior. [Caste specialization in social insects parallels cellular differentiation in mul-
ticellular organisms, depending upon the elaboration of communicative signals in the
form of chemical secretions, and on their selective recognition, followed by
stereotyped responses. These reflexive insect responses to chemical information are
not a fundamental part of the social integration of our species. There is evidence that
pheromones have some socio-physiological impact, such as the coordination of
menstrual cycles. In human society, however, an industry has grown up around
blocking the effect of body odors. Moreover, where behavior is strongly colored by
emotional responses to hormones, social disintegration is just as likely as coordina-
tion. More positive effects are found at the level of interpersonal relationships and the
mutualism of families, which will be discussed shortly. Integration can also be assessed
by the amount of time spent by individuals in contributing to social welfarehigh in
social insects; low in mammalian and bird societies; variable in humans, depending
on social structure. Cells are, of course, committed to organismal welfare except under
pathological conditions. Along with compartmentalization and differentiation,
integration is part of the phenomenon that Aristotle identified as the separation of
offices and concurrence of efforts. This he applied both to the harmonious interaction
of the parts of an organism and to the organization of human society.]
A more recent comparison of social animals and cells appears in Bernard Crespis
2001 essay The evolution of social behavior in microorganisms. It is well known that
many microorganisms form biofilms on a variety of water-covered surfaces such as
underwater rocks, ships bottoms, and human teeth. Biofilms are rich sources of food
for some aquatic organisms. Crespi, however, is interested in integrations of cells in
biofilms that can be compared to properties found in the societies of higher animals.
They may be cooperative, with divisions of labor that provide benefit to all members
of the biofilm. These differentiations involve changes in gene expression, as they do
in multicellular organisms. Biofilms have means of defending themselves from
invaders, including the secretion of acellular polymers that form a matrix which also
protects from desiccation and the infiltration of external toxins. They may be able to
exclude cells of the same species that do not belong to the clone. These processes may
involve intercellular chemical messengers, as may their diurnal rhythms, and the
release of seeding cells at appropriate times.67 Population control is possible in some
microorganism films or colonies through responding to the concentration of chemical
signals that they have released into the near environment, a mechanism known as
quorum sensing.68 In some cases biofilm structure is three-dimensionally complex,
allowing for physiological exchanges, and for the accommodation of complementary
species. Thus, as Crespi argues, biofilms provide shelter, along with nutritional, repro-
ductive and defensive support, as do the constructions of ants, termites, gophers, mole
rats, and humans.
Even without close communication within biofilms, microorganisms may engage in
group foraging, as when myxobacteria attack bacterial prey en masse.69 Pfiesteria
dinoflagellates synchronously release fish-killing toxins, and feed on the cadavers
they are thus a particular menace to aquacultured fish.70 Some microorganisms
cooperate reproductively. For example, while Rhizobium is fixing nitrogen in plant root
nodules, it is incapable of reproduction.71 But if the nodule decays the bacteria return
to full viability. Meanwhile, free-living members of the genus, which may benefit from
ammonia leakage from the nodules, are always in reproductive readiness. Under
limiting nitrate conditions, some cells in cyanobacterial filaments of Anabaena
become nitrogen fixers, losing both photosynthetic and reproductive capacity.72 This
kind of self-sacrifice for the good of the whole is taken further by bacteria such as
Escherichia coli. When they are attacked by bacteriophages they stop synthesizing the
antidote for one of their own poisons and thus commit suicide before the bacterio-
phage babies come to term.73 However, some cunning phages block the response and
prevent the death of the bacteria. Moreover there are always cheaters that get into the
act for a free ride.
I have deliberately slipped into unrestrained metaphorical language, involving
self-sacrifice, suicide, and cheatingthings that humans do. This lack of semantic self-
control is a common failing among sociobiologists and evolutionary psychologists.
Yet Crespi clearly defines what he means by some of these terms:
128 Chapter 3
Altruism: behavior that involves a fitness cost to one individual or cell (the altruist) and a fitness
benefit to another individual or cell (the recipient of the altruistic act).
Cheating: engaging in behavior that exploits the cooperative behavior of conspecifics by
imposing fitness costs on them, while providing fitness benefits to the cheaters. . . .
Cooperation: multiple individuals or cells engaging in a common task for mutual benefit.74
Without quibbling about questionable and undefined terms within the definitions, it
is clear that they are applicable to bacteria and human beings. However all of the
properties that emerge at higher levels are missing from the definitions. The human
complexities of neural conditioning, hormone levels, morals, education, and purpose
are absent. Now, the answer to this objection is that the definitions, as they stand,
inadequate or not, do apply at all levels, and permit commonalities to be demon-
strated at every hierarchical level. If that happens to be an intellectually productive
exercise good and well. However, the next logical step for vulgar reductionists is to
seek genes for cheating, genes for cooperation, genes for altruism, and so on in
bacteria. The hidden agenda of this semantic reductionism is to prove that behavior
can be reduced to those genes from every higher level. And the cheapest shot is that
we too are the victims of those genes. Aristotle compared the division of anatomical
labor in organisms to the responsibilities of governing offices in the city state. In like
manner, the cell theorist Rudolf Virchow compared cellular activity to human society,
regarding disease as internecine warfare.75 Such exercises in metaphor-making spring
from a knowledge of human society, i.e., they are applied from the top down. It may
be heuristic to discover how much putative higher-level complexity exists at lower
levels, yet I do not find any novel conclusions about the nature of cellular interactions
in the examples discussed above. The nature of cellular interactions does not generate
the nature of societies. Moreover, it is counterproductive to semantically reduce the
complexity of human society to something that cells or genes do, in the name of
reductionist ideology. While it is interesting to seek general principles that apply to life
at all its levels of complexity, their discovery should not divert us from comprehensive
analysis and synthesis. At many levels during progressive evolution from the primitive
protobiont level there have been episodic emergences of new associations involving
self-organized complexity, with novel rules of operation. Figurative commonalities like
permeability, integration, differentiation and integration occur in cells, insect
societies, and human associations. However, the similarities that have been listed
above are more of an interesting academic exercise than an answer to any outstanding
biological questions. To understand emergent evolution it is more productive to
identify and understand the differencesthis is where sociobiology and emergentism
part company.
Ricard Sol and Brian Goodwin have recently reviewed the emergent behavioral
properties of social insects in Signs of Life (2000). Here they extend the comparison of
societies and multicellular organisms to the organization of complex brains. Many of
the features are similar in both systems. However, connectedness is a strongly

contrasting property: neuronal interconnections are permanentinsect contacts are
fleeting. Yet ants and termites engaged in nest building will keep coming back to the
same place through positive pheromonal feedback, and local concentration may result
in the construction of pillars and arches, in contrast to the random or chaotic
deposition of building pellets. This may be compared to a long-term memory in a
neuronal network. Both are long lasting emergent phenomena resulting from the
mutual feedback between insect/neuron and the larger environment/brain.76 Such
comparisons demonstrate that although the features of individual social insects or
neurons may be known, behavior at the emergent level of interaction is not reducible
to those features.
Another interesting element in this comparison is the chaotic aspect. Although the
behavior of individual social insects is chaotic, ordered cooperation may emerge, for
example in the form of pillar building. Where it will happen is unpredictable. Sol and
Goodwin suggest that the network of neural connections in the brain also has chaotic
features. By the time of birth, most of the characteristic neural connections between
sensory input and integrating nuclei have been permanently established. Yet there are
billions of additional dendritic contacts, to be added at the unconscious level, which
provide the raw material for thinking and learning and memorizing. To the extent that
they are initially a tabula rasa they are chaotic. Yet a conscious signal, such as a visual
pattern, can create an attractor in that chaosan idea; a thought. With sufficient rein-
forcement, the idea will be stabilized subconsciously, to be retrieved when consciously
stimulated.77
The program of identifying the genetic determination of human behavior that E. O.
Wilson proposed in the last chapter of the first edition of Sociobiology (1975) has been
pursued unsuccessfully. It is easy enough to find genes whose mutants somehow
interfere with some kinds of behavior; but it is outrageously simplistic to declare that
those are the genes for the activity. Nevertheless, tentative suggestions that human
social activities have a genetic basis have become bald assertions of genetic
determinism in Wilsons Consilience (1998). We are told that what we assume to be
freedom of human thought and action is nothing but the commingling of multiple
gene-determined algorithms. By the way, William Whewell (1840) originally defined
consilience as jumping together of knowledge, an intellectual emergence produced
by linking facts and fact-based theory across disciplines to create a common
groundwork of explanation.78 But not much leaping around is possible on a
Procrustean bed built out of a reductionist premise that definitions, facts and theories
have to be cut to fit. Unfortunately, Wilson has meanwhile helped spawn an evolu-
tionary psychology intent on identifying the genetic determination of all human
behavior.
Regardless of any new ideas that might come from system reductions, we should
concentrate on the qualitative differences between emergent levels, and address the
130 Chapter 3
question of how the differences might have emerged. Animals have followed three
different lines of social evolution. Two of these, found in insects and birds, are similar
in that they involve predetermined behavior patterns. The difference between the two
is that some insects have additionally evolved societies that are largely constituted of
non-breeding sibling workers, for example among social bees, ants and termites.
Extreme cases of polymorphism are found in some social insectsagain arising epige-
netically from environmental (nutritional) influences. And the caste structure of their
societies can be manipulated by differentially feeding the larvae. Bird societies
are more flexible, since all of their members are generalists who retain their reproduc-
tive potential. The third type of society is found in mammals, and reaches its highest
level of mutual benefit in humans, who combine a long period of infantile helpless-
ness and family care with societal differentiation. The latter is not stereotyped
and heritable, and it is not all beneficial, especially where the human faculties of
objective observation and logical analysis are inhibited by the stasis of tradition. There
is a tradeoff between these stultifying influences, and their occasional advantages,
along with the general benefits of education. In this regard, Richard Dawkinss (1982)
development of the meme concept of enduring influential ideas is relevant. He feels
that new memes, being subject to competition, are bound to improve through
conscious selection. To me, the lively spark of a Good Idea is equivalent to
an emergence. Its settlement into a persistent ideology with checks and balances
that inhibit further new Good Ideas is equivalent to the establishment of a stable
equilibrium by the syndrome of natural selection. Even in the world of commerce,
this gets in the way of profitable innovation. As to social traditions, politics, and
organized religion, its no wonder we have never emerged from the worst of those. The
passage of memes from one generation to the next has been described as a kind of
inheritance of acquired characteristics modulated by a kind of natural selection. Yet
that kind of inheritance, as Lamarck complained, can get in the way of real evolution-
ary progress. However, this is not to be a treatise on educational philosophy nor
political science, and I will henceforth confine myself to simple familial and social
mutualism.
There can be no question that such mutualism has been an essential part of our
evolution. A pregnant mother has to have sufficient energy and dietary essentials to
bring a healthy fetus to term. Such resources were necessary for the developmental
evolution of humans to reach its present level. Then the post-partum life history
continues with a helpless infant that cannot be independent of parents or social group
for some years. Familial care, or more precisely, maternal care, is not a unique
emergent property of humans, being highly developed in other mammals, and birds,
and to a lesser extent in the other animal groups. Human parental care required a pro-
longation of an existent condition, with the added features of intelligent flexibility
and patience. Hormonal reinforcements made parents more benign, particularly
fathers, who in most other species are conspicuous by their absence from the family
circle, if not an actual threat to the welfare of the young. Exceptions in other
mammals require hormonal changes. Djungarian hamster females and their young
cannot survive without the care of the males, and this is achieved by mutually
attractive hormones. Some such hormonal adjustments are now known for marmots
that mate for life. Oxytocin would appear to make the female fall in love at first sight
and vasopressin does the same for the male. Similar mixological experiments
involving cocktails of oxytocin, dopamine, GABA, serotonin, and norepinephrine
make humans behave like marmots on occasion, and in a less genteel manner. This
tempts some observers to say that human behavior is nothing but the consequence
of gene-determined molecular combinations. But feedback from higher emergent
levels of cognition can influence and override the lower levels.
Human associations are dynamically connected by communication through
language. However, the status of language as a novelty of human evolution is debated
by two camps of linguists and social scientists, who take either emergentistic or
Darwinistic stances. Argument has centered upon the teaching of sign language to
chimpanzees and gorillas, and there seems to be a Darwinist imperative among the
researchers to demonstrate that there is a continuity of linguistic ability from the
chimpanzeesour close biological relativesto humans. If it can be shown that,
despite their anatomical handicap for speech, the great apes have the ability to
assimilate a large vocabulary, and to use word combinations creatively, then the whole
progression of linguistic emergence may be interpreted as a gradual improvement of
that ability, with any small improvement in vocalizing anatomy being naturally
selected and accumulated in accordance with the conventional neo-Darwinistic inter-
pretation. The debate is biased by anthropomorphic public opinion supporting
ape-ability, which has nothing to do with the merits of the arguments, and a lot to
do with wishful thinking about our cute relatives. In contrast, the emergence camp is
accused of being anthropocentrically obsessed with human uniqueness. My own
opinion is that human linguistic ability is a qualitative critical-point emergence
correlated with cerebral expansion and reorganization, one of the major anatomical
emergences of fetalization. It is not a product of quantitative accumulation of little
bits and pieces that have all conveyed sufficient advantage to have gradually produced
human speech.
Along with language came logic. Chimpanzees, gorillas, monkeys, cetaceans, dogs,
cats, parrots, and crows can communicate intraspecifically and with humans by
making symbolic sounds. They also seem able to consciously identify an immediate
problem of survival. And some of them can apparently stop and think, and then act.
Instinctive responses are the fastest responses to such problems, but they lack the
adaptability that can change the reaction in midstream. Yet birds, and even insects,
which depend heavily on instinct, seem to be able to break out of it occasionally with
132 Chapter 3
novel solutions. Even so, humans are the only species that can perceive a problem,
think it out to a logical, and novel conclusion before acting, devise an appropriate
behavioral response, and then execute it, or hold back, according to circumstances and
further analysis of the likely consequences of the action. An intellectual might
approach a problem by rapidly assessing the possible hypotheses, designing thought
experiments to test them, mentally working through the likely results, and finally,
because of all the anticipated failures, do nothing. From the anthropomorphic point
of view, a bright-eyed crow sitting on a branch and cocking its head might be doing
exactly that, but, as the emergentist C. L. Morgan warned, we know from personal
experience that humans do it; it would have to be proved that thats what the crow
was really doing.
Logical abilities contribute immediately to the overall adaptability of humans and
their social groups. Individuals benefit from observing the example of others. The
vocal communication of appropriate action is part of the constellation of emergent
qualities of Homo sapiens. Visual and auditory signals that transfer information have
appeared in many social animals, including insects and birds. But other more sophis-
ticated forms of communication such as sign language have not evolved to any extent
in social animals in the natural environment. In humans, signing comes after the fact
of language, which requires a vocal apparatus, and a range of auditory nuances,
integrated with the innate logico-linguistic functions of the neocortex. Only then
could the invention of signing could be passed down to the great apes under
laboratory conditions.
Alfred Russel Wallace wondered what would be the selective advantage of a brain
that could do calculus long before it was ever needed? However, a prenumerate human
has the unconscious logical ability to analyze rate changes, and voluntarily integrate
this ability with vision and action, when, for example, a running hunter throws a
spear at a prey also on the run. Although it was formally translated by Newton into
calculus, it already existed as an emergent, usable, albeit unformulated quality of the
human brain. It might never be used, and if used would have been subject to modifi-
cation by practice. Another early advantageous use for the emergent big brain was a
quantitative leap in the number of meaningful symbols or words that could be
remembered and vocalized. There was also linguistic framing of logic. Although logic
and an innate grammar, the latter concept itself anathema to Darwinist behaviorists,
occupy different parts of the brain, neuronal connections assure their synergy.
Another aspect of mind also has a social context. Self-consciousness is not necessarily
confined to humans. But we also recognize that others are similarly self-conscious, and
can both empathize with others, and take advantage of that ability. To begin to
communicate linguistically, it helps to be aware that others have the same kinds of
minds, and can perceive the same questions and answers.
Another unique emergent function of the neocortex of Homo sapiens was the
combination of memory with the cultural feature of education. Learning from your
own mistakes is a matter of basic logic and memory, though it comes at a price.
Learning from the mistakes of others is another adaptability with high utility and low
energy cost, even where there is no immediate advantage, and the system operates out
of sight of natural selection. All of these adaptable features were inherent qualities of
the emergent brain of our species, and their potential was further realized by
education and tradition.
Instinctive behavior patterns in insects and birds probably started with a degree of
behavioral flexibility that became genetically assimilated. That is, if any advantageous
activities could be reinforced by gene-based features, the link between the two would
become increasingly fixed. Plasticity was traded off for speed of response. However,
there did not have to be a genetic fixation for the human traditions to degenerate into
the inflexible stasis of rote learning and ritual. The history of medicine provides
numerous examples. Quick-witted folk healers would have been alert to new
knowledge of herbal medicines and toxins, but oral traditions tend to lose the
meaning they had for their discoverers, and to become cluttered with distortions.
Written traditions fared little better. The intellectual flowering of Hippocratic
medicine 24 centuries ago degenerated into a rigid conformity that was briefly shaken
up by the medical founders of the Alexandrian Schools a century later. But medicine
did not enjoy a full renaissance until Galen, after a four-century hiatus. Fortunately,
we humans have the emergent saving grace of humor to help us through strangulat-
ing conventions. This adaptable manifestation of our innate logical ability puts
unrelated ideas together to provide the novel answers and surprised laughter that
finally break us free.
The fixation of human traditions is connected with an issue that is significant for
the formal treatment of evolution by association as a subset of an emergence
synthesis. Since I know of no word that covers all the biological and sociological
aspects of this issue I have to invent symbiostasis. At one end of the association
spectrum, sociobiology recognizes the development of change-resistant dynamic
social stabilitiessocial homeostasis. At the other end of the spectrum, where
endosymbiosis resides, dynamic biochemical and physiological stabilities are
involved.
Symbiosis and Major Evolutionary Transitions
Some of the associations outlined in this chapter are among major transitions in
evolution discussed by John Maynard Smith and Eors Szathmry (1995). For neo-
Darwinists to venture thither is a new salient, and they are to be congratulated for
tackling the difficult thinking involved in explaining natural selection as the cause
134 Chapter 3
of emergent noveltyeven if it sometimes leads them into a logical quagmire. I have

no argument with their estimation of the lapsed time periods, and no fault to find
with their overall historical account. However, I would expect that other ultra-
Darwinists find the following hard to swallow:
We offer the following escape from this paradox [that life originated in a much shorter time than
it took for the eukaryotes to emerge]. During the origin of life, innovations were compared with
relatively inefficient competitors. Established prokaryotes are in contrast vigorous competitors.
Innovations (e.g. loss of the cell wall and origin of the nucleus) are likely to cause disruption and
a transient loss in fitness. Thus, special circumstancesin fact a series of themmust have been
needed for these innovations to become fixed, despite the existence of potentially winning
competitors.79
Maynard Smith and Szathmry explicitly exclude natural selection from the buildup
of generative conditions for the emergence of life, since biological reproduction had
not yet been acquired. Here they argue that protolife thrived when competition was
absent, and when competition strengthened, it obstructed subsequent major
innovations. If that is so, their mandate of explaining transitions in terms of selective
advantage is redundant.
Accepting that the eukaryotic condition found in living organisms did not emerge
fully formed, and failing catastrophic destruction of the competition, the proto-
endosymbioses must have survived through greater adaptability, in environments that
were marginal for existent prokaryotes or where they were not in competition for the
same resources. A reductionistic focus on a step by step accumulation of innovations
never perceives the range of holistic emergent properties that can be simultaneously
generated by integrative complexification. To most Ultras, there is a prolonged evolu-
tionary ferment or struggle for existence and progress is a mere epiphenomenon. In
contrast the emergentist view is that molecular innovations are instantaneous. They
immediately work in the context of the modified whole, or make no difference, or
cause its disintegration. But the primitive prokaryotic experimental tools for such
innovations were limited. Furthermore, the emergence of eukaryotes may have
crucially depended on various prokaryotes being in the same place at the same time,
the place being an interface between aerobic and anaerobic environments. And the
time taken to get to that point was prolonged by the slow buildup of sufficient aerobic
conditions.
Even where competition is brisk, a new wholeness may place emergents beyond it,
or in a position to exploit new environments where the traditional competition fears
to tread. There is no need to adduce an imaginary force that brings pressure to bear,
and picks and chooses from among the old and the new. However, as Darwin well
knew, the very success of novel organisms re-introduces competition among them, re-
imposes dynamic stability, or regression, and constructs barriers to further progress.
Program Notes
In the preceding chapter I issued a checklist of things to look out for at the circus. After
our session at the Symbiosis Arena, we can fill in some of the blanks.
1. Mechanisms that perform in all three rings of the evolutionary circus.

Although we have only attended to one of the rings, mixing and matching of
independent organisms was a crucial part of the original evolutionary process. The
same idea applies in other arenas at the level of gene expression, cellular differentia-
tion, and physiological and social organization. Therefore the phenomenon of
repetition and differentiation of molecules and multicellular associations are also
important, and will be on show in the physiological and developmental arenas.
2. The generative conditions from which emergences spring, and common features of
generative conditions.
So far we have observed the importance of the aggregation of potential symbionts at
appropriate interfaces. Being in the same place at the same time is an important and
highly likely contingency for the establishment of known symbioses, sexual associa-
tions, and interspecific associations. Particular symbioses have unique emergent
properties. But environmental interfaces will be shown to be important and
predictable for physiological emergences as well. Here I wish to re-emphasize the idea
that it may only have been the emergence of an oxidizing environment that provided
the interface for the concentration of the unicells that were to participate in endosym-
biosis, which would go a long way to explaining what took the eukaryotes so long to
emerge.
3. Novelties that catalyze emergences, provided that appropriate generative conditions

are present.
As might be expected, these are mostly unique emergences affecting established
organismal systems, and appropriate to particular conditions of life. As well as internal
adjustments that followed on the heels of the emergence of endosymbioses are many
that were in themselves saltatory novelties. The establishment of nuclei and the con-
struction of chromosomes are examples.
4. Particular contingencies, predictable or unpredictable, which have affected

generative conditions.
In the symbiosis arena these have already been addressed under article 2. One addition
might be the involvement of very large numbers of potential symbionts, as in the case
of sulfur-oxidizing symbiosis or cellulolytic symbiosis.
136 Chapter 3
5. The constellation of multiple functions characteristic of new emergences.

It cannot be emphasized too strongly that endosymbioses established the metabolic
complexity that potentiated plant and animal physiological and epigenetic evolution,
sometimes through regression of the original complexity. The role of symbioses in
founding whole ecosystems, and the role of associations in founding complex
societies, including our own, emphasizes how they have generated multiple functions
indispensable for progressive evolution. These conclusions are also appropriate to the
final article.
6. The course of emergent evolution that has progressively led to greater self-organiza-
tion, independence, and freedom of choice.
After the alpha of the symbiogenesis of life came eukaryotic unicells and then multi-
cellular associations. From their differentiation emerged the morphological and
functional complexities that carried evolutionary progress forward to the omega of the
meeting of minds. Next we will be looking at physiological emergences, which
depended on primordial associations to build the biochemical base for homeostasis. It
will become yet more obvious that the division of the causes of evolution into the
associative, the physiological, and the epigenetic is arbitrary, if convenient. Moreover,
these arenas of causation all exist in an environmental context, and will be found to
depend to some extent, for both their origin and survival, on environmental contin-
gencies.
4
The Physiological Arena
. . . the highest organic development is the most complete division of labour and the most perfect
physiological centralization. . . . Organic progress consists in increasing differentiation and
increasing integration.
J. J. Murphy, 18691
The problem of the organism as a whole is the problem of the origin, development, and
maintenance of the mechanisms of integration in their relation to origin, development and
maintenance of the individual. This is first of all a problem of physiology, not of heredity,
because . . . heredity does not account for the individual, but merely for the potentialities, some
of which are realised in the individual.
C. M. Child, 19242
We have thus arrived at a definition of evolutionary progress as consisting in a raising of the

upper level of biological efficiency, this being defined as increased control over and independ-
ence of the environment. As an alternative we might define it as a raising of the upper level of
all-round functional efficiency and of harmony of internal adjustment.
Julian Huxley, 19423
Physiology is the study of function. Therefore physiological evolutionists must address

the question of how function evolved. We might even ask if it evolved. The
philosopher-biologist J. H. Woodger believed it did not, since all living things shared
the same general metabolic activities in common that allow their persistence in
being.4 All placental mammals, however diverse, have the same physiological organi-
zation and adaptability, which does not diversify in parallel with anatomy. As Darwin
himself said, they share an innate wide flexibility of constitution onto which
adaptations can be grafted.5 Placentals share a good many of their molecular
metabolic activities with their primitive ancestors all the way down to prokaryotes.
Therefore, up to a point, Woodger was right. But Julian Huxley was also right to
recognize the evolutionary significance of a raising of functional efficiency.
Physiological progress enabled the diversification of behavior and anatomy in the
higher chordates and other animal phyla.
138 Chapter 4
Woodger thought that physiologists were not interested in evolution because

metabolic activities were much the same in all organisms. The reverse of the coin is
the indifference of evolutionists to physiology, despite the correlation between
homeostatic sophistication and anatomical adaptive radiation. Darwin remarked,
Practically, when naturalists are at work, they do not trouble themselves about the
physiological value of the characters which they use in defining a group or in
allocating any particular species.6 If the most important physiological features were
held in common across phyletic gaps, it was the grafted adaptations of anatomy that
were of greater evolutionary interest, because their presence could be attributed to
natural selection. J. J. Murphy, who is quoted at the chapters head, understood that
the evolution of organismal complexity was linked with physiology and development,
and St. George Jackson Mivart and E. D. Cope were paying attention. Perhaps one
reason why evolutionary physiology was neglected for most of the twentieth century
was its early affiliation with neo-Lamarckism.
A recent attempt to round the circle of evolutionary causation, beyond ecological
adaptation and population change, incorporates development, yet leaves out
physiology and behavior as its minor consequences.7 But I challenge anyone to
extrapolate from the most perfect knowledge of mammalian embryology to explain
mammalian physiology and behavior, far less their evolution. The physiology of the
embryo and fetus is that of the mature mammal, since, in utero, they enjoy the
homeostasis of their mother. The impossibility of predicting and explaining the nature
of the adult from a knowledge of the embryo parallels the problem of predicting and
explaining the nature of more complex forms from simple, primitive organisms. This
is because evolutionary emergences have novel properties unknown at the lower hier-
archical levels of form and function.
Since evo-devos assume that physiology is a consequence of development,
physiology has been left out of their current agenda. But there is an older historical
reason why physiological evolution has been disregarded: the fascination with
comparative morphology. Gross anatomy is what catches the eye, and its evolution
can be traced in the geological record. Physiological qualities do not fossilize, yet they
support the behaviors that constrain and elicit anatomical change. Another reason for
the neglect of physiological evolution is the historical domination of animal
physiology by medicine, which emphasized its practical relevance to humans. Post-
Darwinian physiologists, such as Claude Bernard, Walter Cannon, and C. S.
Sherrington, took a theoretical interest in homeostasis and the integration of
regulatory mechanisms, but paid little attention to the evolution of such systems.8 A
search for relevant and thoughtful epigraphs took me to where physiology borders on
psychology. In Physiological Foundations of Behaviour (1924), C. M. Child showed a
physiologists appreciation for the organism as a whole, and the same understanding
of persistence in being as Darwin. My third epigraph is from Julian Huxleys Evolution:
The Physiological Arena 139
The Modern Synthesis (1942). Its major theme, progressive evolution, was identified as
improvement in physiological coordination and efficiency. Unfortunately, although
he regarded regulation of body fluid salinity, the amniote egg, the placenta, and
homeothermy, as major physiological emergences, he did not explain their origins.
Others who contemplated physiological adaptability are to be found at the interface
between physiology and embryology. For example, I. I. Schmalhausen, in Factors of
Evolution: The Theory of Stabilizing Selection (1949) agreed that animals had always had
universal metabolic functions, but he also believed that the general features evolved:
Physiologic adaptability is, to a certain extent, a characteristic property of all
organisms. It has arisen simultaneously with life itself and has developed progressively
as the vital processes became increasingly complex.9 Interaction with the environ-
ment and genetic assimilation were important parts of the process. He assumed that
self-organization was perfectly capable of accommodating epigenetic change as well as
physiological novelty, since it had frequently been done over the course of time. And
he was also well aware of the mutual impact of behavioral and physiological
evolution. Moreover, when C. H. Waddington (1957) wrote about the strategy of the
genes, he had general physiology in mind as part of that strategy. In Internal Factors
in Evolution (1965), L. L. Whyte dealt broadly with the coordinative conditions that
integrated developmental and physiological features. Mutations or other changes were
co-adapted within the existing dynamic stability by internal selection.10
David Rollo, an ecologist with an unusual appreciation of physiological evolution,
has commented:
The wisdom of the early naturalists that organisms are intricately balanced so as to carry out a
diverse spectrum of different and specific functions effectively has become formalized in the
ecological concept of the adaptive suite. The essence of this appellation is that each feature of the
phenotype may be adaptively honed by evolution for maximal competence, but the integration
of various aspects may be of even greater importance (i.e. the whole is greater than the sum of
its parts).11
Although comparative physiologists and biochemists will protest with some justifica-
tion that they routinely study physiological adaptations and their energetic efficiency,
they have largely ignored what interested Schmalhausen and Whyte: the evolution of
homeostasis from its rudimentary condition in the first living cells. And that is the
heart of the matter.
By equating adaptability with adaptive suites, Rollo comes too close to inferring
that the elements of complex systems are adaptations that were individually selected,
and that the whole is their sum. Many such adaptations existphysiological special-
izations for particular habits work well in certain environments. Many others
fine-tune the internal dynamic stability of homeostasis, but they do not generate
physiological progress; nor do they offer adaptable multifunctionality. How
homeostasis emerges to higher levels of organization and adaptability is the greater
140 Chapter 4
issue. Michael Conrads Adaptability: The Significance of Variability from Molecule to

Ecosystem (1983) transcends the adaptive suite concept, but dwells little upon the
physiological stage between molecule and ecosystem. However, his later essay The
geometry of evolution (1990) anticipates my present theme:
Why does evolution work? The reason is not to be found solely in the magic optimizing power
of variation and selection. It is as much due to the organizational structure that undergoes the
variation. Evolution works because this organization is amenable to evolution, and because this
amenability itself increases in the course of evolution.12
This reassures us that Conrad is aware of the fundamentally progressive nature of evo-
lutionary physiology. But while he emphasizes the connection of adaptability and
self-organization, he insists that both must earn the right to persist by having some
advantageous trait that can transport all the rest as hitchhikers. A different way of
seeing this is not to separate the advantageous trait from the freeloaders, but to
appreciate it as an integral part of a constellation of features without which it would have
neither advantage nor existence. As I argued in chapter 1, organisms have always had the
physiological right to persist, or to maintain their integrity, except when they have
conducted self-destructive experiments or suffered a natural catastrophe. Any
improvement in self-organization is self-sufficient, bringing a blanket utility that is
already prepared for a range of environmental vicissitudes. It does not follow that
adaptable generalists will always compete better than specialists; but their emergence
in the first place is independent of their future competitiveness.
It might puzzle the reader to note that none of the theoreticians in the above
discussion are or were practicing physiologists. It is certainly bothersome to a physiol-
ogist who has been attempting to explain physiological evolution to students for 30
years, yet has never found a textbook that devotes more than a page to the general
principles of physiological evolution.
Before going any further I want to make a minor grammatical point. Usually the
abstract word adaptability has neither a plural form, nor the company of the
indirect article. It is nevertheless convenient to treat adaptability in the same way as
the similar noun ability. Specific adaptabilities of respiration, digestion, excretion and
so on, in combination with general systems of regulation, add up to all-round adapt-
ability. It seems awkward at first, but one gets used to it, and it avoids circumlocutions.
The Distinction between Adaptation and Adaptability
The performance of both adaptational modifications and adaptable emergents can be

observed in the physiological arena. Adaptation is a genetically fixed and inflexible
quality that is appropriate to certain conditions of the external or internal environ-
ments. If these remain the same, adaptation continues to enhance survival and
reproduction. Extreme adaptations, or particular specializations to the prevailing cir-

cumstances of mature ecosystems, may confer high fitness, and may exclude natural
experiments in adaptability that are unable to compete.
Although internal adaptations have been mostly ignored by selectionists, it is quite
usual for physiologists to think, for example, of a gut being adapted to diet in its
anatomy and enzymological profile. Moreover, some modern comparative physiolo-
gists or physiological ecologists have taken to totting up optimal energy budgets for
physiological qualitiesonly to find that the cheapest is not always the most
competitive. Internal adaptations, such as enzyme variants that function better in
specific pH or salinity conditions than others of the same protein family, are realall
of them can be altered by mutation and thus re-adapt if conditions change. Internal
selection of alleles for these altered proteins tends to stabilize the coordinative
conditions of physiology, or fine-tune homeostasis.
While adaptations are inflexible, adaptability is the quality of an individual
organism to adjust itself effectively in response to internal and external environmen-
tal change. During its own lifetime it thereby maintains its internal milieu, i.e.,
modifies its own behavior, physiology and even anatomy, in the face of environmen-
tal change. Behavioral change also widens environmental range. The environment
need not fluctuate, nor be unpredictable, for adaptability to be brought into play. A
gannets homeostasis allows it to withstand the random blizzards of winter and heat
waves of summer. It may launch itself from the sun-baked ledge of a cliff into flight,
to find its fishy prey, which it then catches by plunging totally into the cold sea. These
environments are quite predictable, and do not change per sethe gannets physiolog-
ical adaptability allows it to stay the same when the environment changes, and do
something different if the environment stays the same. To equate adaptability with
robustness, as is quite common in the current biological literature, is to generalize
too broadly, since highly adaptable organisms may not be robust in the usual sense of
the word, and organisms of low adaptability that conform to environmental change
may be highly robust. Compare, for example, the fate of deep-frozen prokaryotes and
deep-frozen people once they are thawed.
Adaptability is genetically based, in the sense that it needs the information of DNA
that can be translated into enzymes and structural proteins. But adaptability is not
fixed in its phenotypic expression, since the multiplicity of genes on which its
functions partly depend can be switched on or off by organismal and environmental
conditions, and those that are active can have an inhibitory or activatory role within
a hierarchical organization. For example, the voluntary action of writing this passage
includes several layers of operation. Its mental construction and editing involve
creative neocortical intelligence, wakefulness determined by neurotransmitter
molecules, and perhaps emotional coloring by the endocrine system. As a sentence is
142 Chapter 4
transmitted to a written form, sight, excitatory and inhibitory neural control of finger
muscles, and tactile and visual feedback come into play. All of these are governed from
the top down by a conscious decision, and none of them are gene-determined,
although the replenishment of enzymes, neurotransmitters, hormones, and muscles
depends on gene-coded protein syntheses. Nor are most of the developmental
processes that give rise to the organ systems in question directly gene-determined;
they too consist of hierarchically internested molecular, cellular and organ functions.
The greater the degree of adaptability, the more the organism can cope with changing
conditions. Why, in that case, have we paid so little attention to the question of how it so
evolved?
One reason is that adaptation is often used as a catch-all term for adaptation and
adaptability as I have defined them. The word adaptive is also problematical since it
is given the sense of useful, and refers to features that are adaptable (= phenotyp-
ically modifiable or adjustable) and adaptational (= pertaining to genetically fixed
characteristics that are useful in particular environmental contexts). Because it is
essential to make a strong distinction between the adaptable and the adaptational, I
try to minimize my use of adaptive. Unfortunately, physiologists often refer to mod-
ifications of an individual animal as adaptations. When they say we adapt to the cold
by shivering, nobody bothers that it confuses two fundamentally different kinds of
response. When we get cold, the gene for shivering is not switched on, since it
doesnt exist. Yet popular interpretations of molecular biology, which professionals
sometimes encourage, would have us believe that there is a gene for everything. And
if adaptability is arbitrarily treated as a subset of adaptation, it becomes easy, not only
to confuse two distinct categories, but also to lose the most important one. Michael
Conrad (1983) says that it is necessary to develop a theory of fitness that does not
have to answer every question about the functional value of this or that adaptation.
Conrad continues:
In fact, this is quite impossible because particular adaptations are so particular and specific.
However, this is not true for adaptability. This is because adaptability is adaptation to the
uncertainty of the environment, therefore adaptation is something which can in fact be charac-
terized in a very general way, independent of the specific features of different environments.
Moreover, adaptability and also reliability (or adaptations for coping with noise) are just the
adaptations which are crucial from the standpoint of determining the directions of evolution, for
not only are they what determines whether some particular biological organization has the right
to persist, but they also encompass the genetic search strategies which determine the probability
with which these different organizations come into existence.13
Conrad, a stickler for formal usages, defines adaptability as the ability to cope with
the unexpected disturbances of the environment, and reliability has the special
sense of the ability to cope with internal noise, or shutting out irrelevant perturba-
tions within systems, whether they be cellular, organismic, or pertaining to

populations, communities, or ecosystems. I have no fundamental objection to either
of these definitions, and applaud his clear recognition of the importance of adaptabil-
ity for determining evolutionary directions.
Nevertheless, Conrad also sees adaptability as adaptation to the uncertainty of the
environment [emphasis added], which rationalizes adaptation as the higher category
and adaptability as the subset, when he should instead be explaining the mystery of
how the challenge of uncertainty can be met. Since he obviously finds a real
distinction between particular adaptations and adaptability, his semantic reduction of
adaptability to adaptation is not careless, but an evasion of the difference, perhaps to
make his comprehensive fitness theory tidier. Yet, sweeping adaptability under the rug
of adaptation is not real theoretical tidinessout of sight is not out of mind if the con-
tradictions are fighting like cat and dog under there. Subsuming adaptability under
adaptation solves Darwins problem by making persistence in being an adaptation
and therefore amenable to natural selection. And that of course will reassure neo-
Darwinists that what they previously neglected as an exception can be harmoniously
subsumed, without carrying the analysis any further.
A parallel problem arises when physiological adaptability is equated with the
variability of populationsas Conrad does in the very title of his book: Adaptability:
The Significance of Variability from Molecule to Ecosystem (1983). This ensures that adapt-
ability can be filed and forgotten in the same box as genes that may have multiple
alleles, or a population that has broad genetic variations or polymorphisms. That ploy
allows population biologists to ignore physiological adaptability and get on with bean
counting: a case of lets not do it but say we did. The adaptability of an organism
the ability to modify itself or its behavior in direct response to environmental or
internal changeis a property that is qualitatively distinct from variability in
populations. And if popular usage confuses categories it should be corrected. Conrad
can keep variability as a property of populations, but I am going to treat adaptability
as an exclusive property of organisms, and deal with it in my own terms with
particular reference to the physiological arena.
Since I have been largely concerned in the adaptability at the level of physiological
organs, and with the general adaptability of the organism to its environment, I have
ignored a significant aspect of Conrads Adaptability: the adaptability of biological
molecules to one another. Marc Kirschner and John Gerhart compensate for this
deficiency in The Plausibility of Life: Resolving Darwins Dilemma (2005), in which they
demonstrate how the adaptability of regulatory mechanisms can not only ensure that
the organism survives biomolecular change but also accommodate environmental
effects as part of epigenetic and hence morphological change. The significance of the
latter will be raised in chapter 9.
144 Chapter 4
Modes of Adaptability
Toleration and Accommodation

Some organisms can tolerate internal environmental change imposed by external envi-
ronmental change, up to a limit. But tolerance is usually accompanied by behavioral
adaptability such as shutting out the environment, or escaping from the hostile zone.
Tolerance also may be supplemented by the kind of adaptability known as accommo-
dation, where, despite internal change imposed by external environmental change,
physiological responses allow the organism to function adequately. The most sophis-
ticated kind of adaptability is homeostasis, a stable dynamic equilibrium that keeps the
internal milieu relatively constant, despite external environmental changes.
Many marine animals that live on the seashore tolerate the diluting effects of fresh-
water runoff, periodic drying, heating and cooling, and when conditions become
intolerable they shut themselves off from the environment, or walk, run or swim
away. But they often have accommodatory mechanisms better than mere tolerance.
For example, a species of bivalve lives on the western beaches of my neighborhood
fjord, Saanich Inlet. Nuttallia obscurata, called the varnish clam because of its shiny,
yellow-brown, outer protein coat, was introduced from Japan or Korea about 20 years
ago and has already spread far to the north.14 Its larvae are attracted to fresh water
flushes and settle in large numbers in the high tidal zone, some of them even
burrowing in the bed of an outflowing rivulet. I regularly find adult specimens alive,
but tightly closed, in the lower reach of the stream. It seems as if the constant presence
of fresh water finally makes them decamp and resettle further down the beach where
the water is saltier. Their adaptability consists of a combination of clamming up,
locomotory mobility, passive drifting, and accommodating to fresh water. They also
have unusually versatile feeding habits, including ciliary feeding with the foot, a habit
usually confined to juvenile bivalves. Their choice of the upper shore has separated
them from most of the other clams, so they are free of interspecific competition for
space, although they run the risk of discovery by terrestrial predators.
As an example of accommodatory mechanisms in animals subject to internal
change brought about by external change, some salmonids have a suite of kinases,
energy conversion enzymes that have maximum efficiencies at different temperatures,
and so can continue swimming at the same speed when they get warmer or colder.
Seasonal temperatures change much too fast for random gene duplication and
mutation to keep up, so the suite of enzymes had to be already in place to be effective
when the fish subjected themselves to environments with a fluctuating temperature
regime.
Homeostatic stability of the internal milieu through the operation of regulatory
feedback mechanisms makes existence in different environments possible. It also
potentiated brain development, the evolution of intelligent behavior, and the

emergence of mind. These, in turn, supported homeostasis by inventing clothing, fire,
houses, scuba gear, and vacuum-proof spacecraft.
Although the scope of behavior in animals other than ourselves usually has to be
limited to what homeostasis can deal with effectively, there are exceptions of
toleration, where some homeostatic elements are temporarily or permanently
abandoned. For example, humans, like many other warm-blooded vertebrates,
accommodate to strenuous exercise by accumulating an oxygen debt. That means that
the muscles switch to anaerobic respiration and temporarily build up lactic acid.
During this accommodation period, oxygen levels, metabolism, and lactic acid con-
centrations are all different from the resting equilibrium. When exercise stops, and
sufficient oxygen is present, the homeostatic balance is restored.
There are more striking examples of temporary regression of homeostatic regulation.
A dehydrated camel allows its core temperature to fluctuate several degrees from its
normal set temperature. Relaxation of homeothermy into toleration of change is an
option that saves several liters of body water per day, which would otherwise be
sweated off to keep the body temperature down to normal. It is also contingent on a
climate with cool nights, allowing the excess body heat to be radiated off, leaving the
camel to start the day cold, and characteristically grumpy. Even more exceptional is
the eusocial naked mole rat Heterocephalus glaber, which lives in burrows that have a
high, stable temperature. It has largely abandoned endothermic heat generation, with
the advantage of significant savings in metabolic energy. R. D. Alexander (1991) sees
this in the larger context of an odd constellation of attributes including nakedness,
slow growth, ectothermy, burrowing life-style, eusociality and specialization on
underground tubers . . . unlikely to be understood unless they are considered
together.15 This is the kind of holistic, or interactionist viewpoint necessary to
understand the emergence of physiological novelty, which comes out of an array of
interrelated generative conditions, and confers a multifunctional constellation of new
ones.
Homeostasis
The highly adaptable condition of mammalian homeostasis was first described by the
physiologist Claude Bernard as a constancy of the internal milieu that conferred la vie
libre, or independence from the external environment.16 He did not mean that the
internal environment was rigidly fixed, knowing that continuous physiological
adjustments were needed to maintain the apparent constancy. Bernard was not just
making a vague generalization, for he had analyzed specific components such as the
regulation of blood sugar. In The Wisdom of the Body (1932), the physiologist Walter
Cannon coined the word homeostasis for this physiological condition. Like Bernard,
Cannon was indifferent to evolutionary explanations.
146 Chapter 4
In teaching comparative physiology, and trying to explain the evolution of the

physiological steady state, I raise the homeostasis paradox. Given that the internal
milieu has changed historically in its salinity, temperature, oxygen capacity, and
organic content, how can homeostasis evolve, if during the process it progressively
becomes more change-resistant? Alexei Severtsov was fascinated with such problems
of the evolution of adaptability, as was his junior colleague Ivan Schmalhausen.17 A
few decades later, the theorist C. H. Waddington realized that a parallel paradox
existed in developmental evolution. The consistency of developmental functions,
which he called homeorhesis, resists embryonic change in the same way that
homeostasis resists physiological change. Waddington came to the same conclusion as
Schmalhausen: changes in stable internal systems were most likely imposed from
without.18
Physicochemical parameters of the internal milieu have historically been disequili-
brated and changed in response to environment, especially in freshwater and terrestrial
animals. This straightforward environmental impact was named physiogenesis by
the neo-Lamarckist E. D. Cope. Among those physicochemical features, body fluid
salinity, oxygen content, temperature, and mechanical stresses have been changed by
the environment over the course of time. Ultimately standards were set and regulated
as part of organismal homeostasis. These features were initially changed by the
environment, and did not evolve in a biological sensewhat evolved were the
homeostatic mechanisms that regulate them, especially the hormonal and nervous
systems that increase overall adaptability. Those went on evolving after the physico-
chemical factors had reached their final set points. The unanswered question is How
did the organism genetically assimilate what began as an ontogenic effect? The
conventional hypothesis is that any genetic or epigenetic change that complements
the ontogenic effect would be marginally advantageous since it would give the
organism greater freedom from its environment. But this is paradoxical. Why go to the
lengths of genetic assimilation which is not per se advantageous if the organism is
consistently and persistently exposed to the required environmental stimulus at no
energetic cost?
Physiology, as the examination of function, combines the study of internal
organismal biochemical activities and functional anatomy. But it should be clear from
the previous discussion that physiological evolution also needs to be understood in a
behavioral context. An animal might stay where it is while the environment changes
climatically or catastrophically. Alternatively, it may go to a new environment that
will affect the evolution of its lineage. This requires complex behavior, which in turn
depends upon the adaptability of underlying physiological systems. Here is where
genetic accommodation shows its worth, even when the organism has no need to
depend on it until behavior and changed environment so dictate. There would be no
future in exploring an environment where survival was impossible. Such adventurism
is thwarted by stereotyped behavior that is predictably fit for the prevailing conditions
of life, genetically based and rigorously selected; but it leaves little scope for accident
and experiment. The evolutionary alternative is to increase physiological adaptability
and freedom of behavioral choice. Along that route, intelligence may emerge, and the
dangerous streak of curiosity kept under conscious control. .The grounds of the idea
that behavioral change results in ontogenic change and thus catalyzes evolutionary
change is discussed by Gilbert Gottlieb (1987) as an essential component of a genuine
evolutionary psychology. Gottlieb, like the historical predecessors he mentions, does
not emphasize physiological adaptability as the foundation of such behavioral
experiments.
The feedback relationship between internal physiological functions and externally
directed behaviors have changed the epigenetic and mature internal milieu, made
physiology more complex, and led to further behavioral evolution. Since behavioral
studies are commandeered by ethology or comparative psychology, and early develop-
mental functions are studied under embryology and epigenetics, a more
interdisciplinary approach is needed to integrate development, physiology, and
behavior. Roy Pearson (1986; 2004) has contributed to such a synthesis by merging
homeostasis with developmental physiology as homeodynamics. However, I will
keep it simple for the time being, and try to make the most of physiology in its own
right.
It is an oversimplication to see a physiological organ system as an adaptation to
ecological conditions. It must also be appreciated that increased complexity of
regulatory systems can provide general-purpose improvements, regardless of current
exigencies. For example, a neo-Darwinist explanation of nerve myelination might be
that first one axon of particular adaptive value was myelinated, and subsequent myeli-
nations were selected according to their contribution to Darwinian fitness. In contrast,
myelination of nerves could be seen as an emergent phenomenon involving much of
the nervous system, activated by an epigenetic change that made all of the accessory
glial cells act in the same way. It was not only a specific escape response to a particular
predator that was speeded up (and then selected). Multiple sensorimotor functions
were affected. Multifunctionality is an important aspect of the evolution of more
complex homeostatic systems.
Multifunctionality
Most emergent systems have multiple functions, some of which may confer
competitive advantage. Others may later increase the organisms ability to survive
changing environments. They are a mixture of qualities that existed prior to
emergence, or came into being with the emergencenot post hoc adaptations to
environment. They were there from the start, unnoticed by natural selection (i.e. they
do not have differential effects on survival and reproduction), and hence they are
148 Chapter 4
ignored by neo-Darwinists who are on the lookout only for the key adaptation that
constitutes the explanation. Conventional usage for such pre-existent qualities that
have novel adaptive powers is the awkward word preadaptation, which suggests that
adaptation can anticipate future conditions. A better word is exaptation, which
implies that a primitive structure that served a particular function can convert to a
novel function.19 But simple exaptation needs deeper analysis to bring out inherent
multifunctionality. For example, the statement that a primitive fish lung is a preadap-
tation for buoyancy, can be replaced with as its respiratory function was
unnecessary it became exapted for buoyancy. But although it is a semantic
improvement it is not a comprehensive argument. By simple physical principles, a
lung at its inception is already a buoyancy organ, before the accoutrements of a swim
bladder have been added. Not only were lungs bifunctional, they were differentiated
duplicates of gill pouches that originally had multiple functions of respiration,
feeding, and metallic ion uptakeall derived from an alimentary tract that had many
other selectively absorptive powers.
The gut is a major conduit of exchange between the internal milieu and the external
world, being formed of absorptive endoderm in contrast to the relatively impermeable
outer ectoderm. Not only is food digested and absorbed, but salts, water, and
respiratory gases can be exchanged. This constellation of functions existed
immediately when guts first emerged. In the deuterostome line from which the
chordates arose, a filter-feeding apparatus that doubled as a respiratory organ was
added at the anterior end of the gut. It persisted in the primitive jawless fish, and is
still seen in the ammocete larvae of lampreys. Its iodine-absorbing endostyle groove
became the vertebrate thyroid gland. From the tops of the gill pouches was derived the
thymus gland, which in fish retains a segmental appearance. The ciliated slits, which
had the dual role of food filtration and ventilation, became specialized as gills. As well
as exchanging oxygen and carbon dioxide, gills retained salt-absorbing or salt-
excreting functions, and complemented the excretion of nitrogenous waste. Then,
from posterior embryonic gill pouches, the first simple air sacs emerged as lungs and
swim bladders. Our own lungs still contain epithelia derived from the endoderm of
the gut.
As another example of multifunctionality, mammalian hair glands secrete fluids
that could immediately act as coolants, nutrients, and hair conditioners. The
emergence of those secretions was correlated with dental differentiation, and the
anatomical flexibility needed for grooming. If an organ is multifunctional to begin
with, its morphology may diverge in several different specialized directionshair
glands might become mammariesor it could remain unspecialized, adaptable, and
multifunctional. Multifunctional adaptability is particularly important in stressful
fringe environments, or at interfaces between different environments.
Life at the Edge

Conventionally, it could be argued that in unstable fringe environments natural
selection would favor adaptability and remove inappropriate specialization. Edge effect
(Cook, 1961) is an orthodox proposition that adaptable types originate at peripheral
environments as a result of reduction in interpopulation migration and protection
from the diluting effects of the larger gene pool. Their survival is reinforced by coad-
aptational differences presented by unusual biotic and physical factors. But edge effect
is based partly on the concept that in evolution nothing can happen unless there is a
selection pressure to force it. The less conventional idea of Schmalhausen and Belyaev,
namely that in fringe environments stress destabilizes the physiology of organisms,
and allows more room for physiological maneuver, would seem to argue that the
fringe environment is where evolution happens. This would miss the point that
adaptable organisms already exist in the parent population. Adaptability can become
more sophisticated autonomously in the population at large, and have novel manifes-
tations that might have incipient physiological advantage in stressful environments,
if the more adaptable types can get to them. As far as plants are concerned, random
distribution of seeds or spores makes their destiny a matter of luck. And those that are
sufficiently adaptable may be lucky enough to fall on stony ground, where there is less
competition for space. In contrast, animal distribution through exploratory behavior
is self-directed for those that are more generally adaptable. Some of them may also
have incipient superiority on stony ground, or other stressful conditions.
Schmalhausen had already displayed a holistic view when he wrote the following:
Physiologic adaptability to variations in the external environment enables organisms to migrate

more freely and to conquer new places in nature to a much greater extent than does morphologic
adaptability. This occurs because the former is established much more rapidly, and is character-
ized by quickly and easily reversible reactions. Hence, physiologic adaptability denotes a
considerably more extensive eurybionty than does the capacity for adaptive [adaptational] mod-
ifications. Organisms can live and multiply under extremely diverse conditions. In view of the
rapidity of physiologic adaptation [adaptable response], especially of behavior, an organism is
transformed relatively easily even when biotic conditions vary (within definite limits). Other
conditions being equal, this means a diminution in the intensity of elimination, and an increase
in the number of individuals of the given species but within the limits of the physiologic adapt-
ability of the species.20
Schmalhausen went on to say that physiological adaptability also accommodated

epigenetic change.
My own thinking about these matters was catalyzed by J. W. Beaments 1961 review
essay. The role of physiology in adaptation and competition between animals. He
concluded that general adaptability, especially in insects, would make it possible for
them to be far more widely dispersed than is usually found in nature. The egg of the
cabbage white butterfly Pieris brassica can hatch and go through several molts as a
150 Chapter 4
caterpillarunder watergiven a supply of cabbage. Beament was particularly

interested by the structure of the insect cuticle, and concluded in a 1964 report that
the orientation of an internal monolayer of wax molecules was sufficient to provide
waterproofing. At transition points (usually above 30C), thermal disruption of van
der Waals forces that hold the wax molecules together lead to sudden water loss. The
pupae of the cabbage white have additional protection in a cuticular surface wax
monolayer that keeps them waterproof to 60C. Beament also established that in
aquatic insects the monolayer was inverted, so that water was kept out, and postulated
that the hydrofuge waxiness of the tracheal system and its spiracles could have
allowed aerial respiration in the aquatic ancestors of insects. Aquatic insects often
carry a bubble of air with them which acts as a physical gill. As oxygen in their
tracheae diminishes, it is replenished by dissolved oxygen from the environmental
water. Because the nitrogen in the bubble is not used, and diffuses into the water very
slowly, it keeps the bubble-gill stable, so that the insects do not have to constantly
surface to replenish it. Despite the general perception of insects as little automata,
many can adjust their behavior. Darwin knew that without any respiratory or
locomotory specialization some proctotrupid wasps can submerge themselves
underwater for up to four hours, swimming with their wings.21 Thus, the emergence
of lepidopterans with aquatic larvae is not unimaginablethe early stages of the insect
life cycle are where most of their evolutionary plasticity resides. But what they would
need is freedom from competition and predation from insect and other specialists
already in the water, and perhaps some kind of aquatic cabbage to get them started. If
I were to retitle Beaments original essay, I would call it The limitations imposed by
adaptation and competition on physiological adaptability.
Schmalhausen combined two fundamental types of emergence. The first was
intrinsic increase in complexity that improves general physiological adaptability. The
second was the autonomization of extrinsic factors, or what might now be described
as the genetic assimilation/accommodation of useful, environmentally induced,
phenotypic changes. Subsequent mediation of both of these types of emergence was
by the fine-tuning of internal physiological organization, through co-adaptation of
the constituent mechanisms. This aspect of stabilizing selection operated on the
physiology of organisms, and by omitting that aspect, population biologists render it
theoretically jejune. Physiological stabilization was an endogenous process that would
occur under any circumstances. But Schmalhausen did not exclude more strictly adap-
tational innovations, physiological or anatomical.
What came out of Schmalhausens synthesis of intrinsic and extrinsic emergences
was that the resistance of dynamic stability to change could be overcome. And in
extreme environments adaptable organisms stood a better chance of evolving further.
Adventurous organisms have to be adaptable in advance of exploring new stressful
territories. Filters do not exist for them, but competing conspecifics or congenerics are
excluded, so that a novel genetic and physiological and behavioral mix could then
destabilize the norm. Therefore, while this discourse incorporates some Darwinist and
neo-Lamarckist thinking, it leaves out selection pressure, and the inheritance of
acquired characteristics. When Lamarck said the organism responded to a need, he
could have been anticipating the idea implicit in selection pressure. But the organism
does respond to its environment, not just through physiogenesis but through its
anatomical, physiological and behavioral flexibility, and that finally has an evolution-
ary effect. These points are illustrated by the following case histories of animals at the
edge.
The furry-footed Djungarian hamster Phodopus campbelli inhabits desert regions of
Asia that have long, cold winters and short, warm summers. Kathy Wynne-Edwards
and her colleagues have thoroughly studied reproductive hormonal physiology, repro-
ductive behavior, parental care of the young, and foraging behavior.22 And they draw
on existing data for excretory physiology, predation, and general features of the local
environment. Phodopus campbelli has an unusual constellation of endocrinological
and behavioral qualities that allow it to survive in conditions of low temperature and
lack of water that would be stressful to most mammals, including its nearest relatives.
While subject to wild predators, Phodopus campbelli avoids competition with the
congeneric Siberian hamster Phodopus sungorus. Homeothermic animals need water,
and lactating mammals, living in burrow microclimates during a short summer, get
hot and desiccated. With an excretory efficiency like that of the more familiar desert
rat Dipodomys, Phodopus campbelli can go without free-standing water, but has to
forage for long periods of the night to find enough seeds and juicy insect larvae to
provide energy and water. Paradoxically, the cold-adaptations, including fur and fat
insulation, are necessities of survival in winter, but liabilities during the short, warm
breeding season, because the lactating female, in close contact with her pups, is likely
to overheat and dehydrate. Hormonal modifications in females of the species,
especially in post-partum progesterone production, attract the male to be constantly
present and available to keep the young warm, while she departs to forage and cool
off. The male has a hormonal role to play too, since pregnancies are usually aborted if
he is not close by most of the time. He has the additional role of delivering the pups
and then cleaning them up.
This case is especially interesting as a natural example of the destabilizing selection
that D. K. Belyaev identified in domestic Arctic foxes, and which I introduced in
chapter 1. Belyaev was well aware of Schmalhausens quest for conditions that would
disequilibrate the balancing selection that blocked evolution. Tameness had been the
main factor in the choice of foxes for breeding stock and along with it came unusual
reproductive cycles sensitive to hormonal features distinct from those of wild foxes.
Thus, the artificial conditions of the farm, which necessarily included freedom from
152 Chapter 4
competition, predation, and climatic extremes, destabilized the kind of dynamic

population equilibrium found in the wild. Here, the agents and differential conse-
quences of natural selection were absent.
As Belyaev inferred, we should be looking to situations where wild populations,
societies, or simply pairs, living in stressful conditions, have a behavioral and
hormonal interplay that causes a constellation of changes that reduce stress, and in
some instances increase cooperation. Stress is not a selection pressure that has caused
the changes. Those were incipient in the ancestral population; the behavioral and
physiological interactions of the more exploratory individuals brought them out, and
the absence of competition was a more significant factor, allowing the changes to persist.
Wynne-Edwards judged the Djungarian hamster to be an appropriate model for
Belyaevs destabilizing selection, when I broached the subject with her. However, she
puts Phodopus campbelli into the boxes of proximate and ultimate causation,
suggesting how it became differentiated from its closest relative P. sungorus by a variety
of antagonistic selection pressures, extreme environment being the ultimate selective
force. It is more parsimonious to think about furry-footed hamsters in their own right.
They can live at an environmental edge because they have all the emergent qualities
of placentals. The ancestors of Phodopus campbelli already possessed the adaptabilities
needed to push the envelope: water regulation, insulation, adipose tissues, a
modifiable hormonal output, and a range of adaptable behaviors. They could avoid
persistent predators by nocturnal foraging, and, as they pressed on, competition for
food from their own species and other small mammals was reduced. Some might have
already had a sufficient rudiment of male and female togetherness that could be phe-
notypically reinforced by positive feedback: the more cuddling the more hormones;
the more hormones the more cuddling. Not much genetic assimilation of appropriate
hormonal variations would be needed to reinforce what already existed. Others of the
ancestral type would have failed to reproduce under the harsh conditions. It is more
to the point to examine the qualities that ensured the success of P. campbelli than what
natural selection did to others that lacked them. The Siberian hamster, P. sungorus,
stayed behind in more benign conditions, but some individuals show incipient traces
of the hormonal requirements for success in colder, drier conditions. Furry-foot
demonstrates the generalization made earlier about naked mole rats, which have also
found a way to succeed under environmental stress. We must appreciate the full
spectrum of generative conditions and the full constellation of emergent features.
Though it is tempting to find a key innovation that was selected, there is in these
hamsters lives a web of causality, involving behavior, environmental feedback,
homeothermy, hormonal changes, and hamster houghmagandy.
Another commonality between hamsters and other animals living at extremes is
family togetherness through hormonal mediation. The emperor penguin, Aptenodytes
forsteri, raises its young close to the South Pole. Females lay their eggs and then head
north for the open sea. Their mates incubate the eggs during the dark freezing winter,
and cooperative huddling keeps them up to 50 percent warmer than they would be on
their own.23 The penguin females, fat from feeding in the faraway ocean, finally take
the long trudge necessary to relieve their babysitters in the nick of time.
In an environment at the opposite climatic extreme, we find eusocial naked mole
rats. (That is, they live in extended familial association of parents and siblings.) Their
interactions are modulated by hormones and behavior, although, unlike hamsters,
bonding and mutual comfort seem hardly appropriate descriptions for mole rat
cooperativity. The queen actively suppresses sexual reproduction in other mature
female colony members. Detecting those that are in estrus, she aggressively jostles
them until they are sufficiently stressed to go into anestrus. However, when she is too
heavily pregnant to be a bully, some of the non-breeding females come back into
estrus, so that they are ready to mate in case of accident to the queen. Mole rats in
general are confined to burrow systems that have a stable temperature, and their
homeothermic abilities have regressed. Being under heavy predation, they are short-
lived, and they depend on their social arrangements for survival.24
It is hard to see what more animals such as Djungarian hamsters and naked mole
rats could do, apart from minor adjustments. Theyve gone about as far as they can go.
Schmalhausen had a word for that: telemorphosis. It is now appropriate to
distinguish between two kinds of stressful, edge environments. There are boundaries
that provide some respite from competition for physiological opportunists, but which
physically resist further encroachment. These include polar surface conditions, and
the diminished oxygen levels of the upper atmosphere. Bacteria, of course, prove this
rule, since they can survive in outer space for a while, as well as living at temperature
and pressure extremes. But their robustness is different from the vulnerable adaptabil-
ities of insects, birds and mammals. On the other hand some interfaces were
temporary barriers: between anoxic and oxygenated; between salt and freshwater;
between water and land. Their penetration required a prior quality of adaptability, and
diversifying evolution was subsequently the result.
The gannet is an example of an adaptable animal with sophisticated homeostasis
that allows it to stay the same when the environment changes, and also to change its
environment spontaneously, as when it dives after fish. A more striking example of a
bird that exposes itself to stressfully extreme environments is the Arctic cormorant.
One would think that temperature homeostasis would be utmost importance to it. Yet
subdermal fat insulation and the secretion of preening oils have regressed in that
cormorant species. Not only do they get colder faster, but also their plumage is more
wettable, and they have to hang out their wings to dry in freezing temperatures after
a dive. On the plus side, reduced insulation means reduced buoyancy, and cormorants
can dive after prey to greater depths with less effort. Owing to the anomalous
properties of water, the deep temperature of Arctic seas is not much colder than that
154 Chapter 4
in more temperate zones. The potential trouble arises from having to expose a wet
body surface to dry off in subzero air, where the sacrifice of body heat is unavoidable.
Yet diving for about nine minutes a day satisfies the cormorants usual nutritional and
thermoregulatory needs. In the absence of competition from other birds, they are able
to tap a major resource of high-energy, fatty food. Their adaptability sustains them
even in the absence of apparently crucial adaptations for living in the Arctic.25
Complexity theorists use metaphors like life at the edge of chaos to refer to
biological molecules that persist through being not too stable and not too unstable.
Metaphorically, organisms too can exist at the edge of chaos, between stable
ecosystems and adjacent disruptive environments. Those that can meet the unpre-
dictable challenges of physicochemical extremes elude the competition that operates
in the dynamically stable conditions of the ancestral environment, and so can escape
from the hypostasis of natural selection. Fish in estuaries, for example, could histori-
cally acquire new food resources, occupy new living space, and escape from predators,
and competition, if they were willing and able to make the final leap. Fringe environ-
ments that are only marginally different from the parental ones are still more likely to
be habitable by the most adaptable types. Here, they can congregate, and test the
unexploited adjacent environment. Once they have passed into a new environment,
they can diversify without hindrance from the agents of natural selection. As the
pristine environment fills up, the radiating lineages become more and more
specialized, and the sap of originality dries up. At the present time, interfacial environ-
ments are occupied by specialists that should not be taken as models for adaptable
transitional animals on the verge of invading the adjacent, pristine land. But the
specialists do give us some clues to the adaptabilities of those that went further with
their explorations.
Once the original adventurers passed through the interface and into a new
environment, different physicochemical conditions were imposed upon them, and
these potentiated further advances in adaptability.
Physiogenesis
One of the significant generative features of adaptability is physiogenesis, physico-
chemical change imposed on an organism by the environment. Once animals
acquired body cavities and blood vascular systems, their body fluid buffered the weak
cellular homeostasis from the insults of the outside environment. But initially the
internal milieu conformed to the physicochemical nature of the marine environment.
As long as the sea remained constant, so did the body fluid. In contrast, animals near
the seashore, or near influxes of freshwater, were affected by environmental fluctua-
tions and this is one of the preconditions for the further evolution of adaptability. This
is the definition of physiogenesis first given by neo-Lamarckist evolutionist Edward
Cope. Ivan Schmalhausen complicated the issue by adding the biological ability to
deal with such change, but the original is more straightforward. Physiogenesis is not
a metaphor like selection pressure, but a real physicochemical cause that acts
immediately and continuously, eliciting tolerance, accommodation or the response of
homeostatic mechanisms. The next step is for an internal dynamic stability to be
established that minimizes the energy drain, while preserving responsiveness. Here
internal selection or co-adaptation is involved, as Ivan Schmalhausen and L. L. Whyte
proposed. But Schmalhausen realized the internal stability, both in physiology and
development could be a barrier to further evolutionary change. His senior colleague
Alexei Severtsov coined a catch-all termaromorphosisfor the whole spectrum of
changes that started with the destabilizing influence of physiogenesis and ended with
improved adaptability. He believed that aromorphosis came in emergent waves,
alternating with slack periods of adaptational evolution, a kind of physiological
punctuation also favored by the saltationist K. Beurlen.26
But where is emergence located in the syndrome of aromorphosis? The organism
might have literally emerged, say from water onto land, to be immediately affected by
dehydration, gravity, new mechanical stresses, high oxygen tensions, and fluctuating
temperatures. But the event was made possible by physiological adaptability that had
earlier emerged in the transitional organism, probably before it got to the edge. Maybe
components of the unexploited adjacent environment intruded sufficiently to
influence the process. Adaptability supported the behavioral choice that led to the
environmental change. Then physiogenesis immediately caused internal changes for
which adaptability could be adjusted and then advanced. Existing physiological
functions, locomotory anatomy, behavior, and inducements of food or escape from
predators are the generative conditions for the shift. Physiogenesis, and adjustments
to it, then generate conditions for emergence to a higher level of adaptability, such as
a critical-point allometric growth of the central nervous system. These all happen to
responsive organismsnot to temporary bags of genes.
Genetic Assimilation of Physiological Change

Genetic assimilation is Waddingtons term for what Schmalhausen called autono-
mization: a consequence of change imposed by the environment.27 I will extend the
discussion of this topic in a historical context in chapter 5. Although genetic assimi-
lation implies a genetic fixation of an ontogenic characteristic, it is not as Lamarckian
as it seems. It combines the direct effect of environment with the syndrome of natural
selection: but only if the organism had the original capacity to expose itself to new
conditions and be affected by them. Fundamentally it proposes that any phenotypic
change imposed by the environment that aids the organisms survival can be further
enhanced by the selection of any gene-based mechanism that reinforces the change
assuming that such a mechanism already exists. Molecular experiments can produce
novelties that are appropriate to new conditions. The evolutionary process begins,
156 Chapter 4
either when the environment changes spontaneously, or when the behavior of the
organism subjects it to new conditions. The more the adaptable its physiology the
more likely is its survival.
When an animal is physiologically adaptable enough to experiment behaviorally,
physiogenesis may be the next effect: environmentally imposed change or constancy.
Then there are internal modifications and adaptations appropriate to the new
condition: for example expanded enzyme suites with optimal activity at a given
temperature, or in a particular electrolyte medium. At that point homeostatic
regulatory novelties that keep the condition constant in the face of change have high
fitness. Behavioral exploration, supported by improved physiological adaptability,
may effect functional-morphological change. The process therefore combines physio-
genesis, behavior, the emergence of adaptabilities, adaptations, and possibly
orthogenesis. The provision of genomic change that constitutes genetic accommoda-
tion of phenotypic change is not simply a neo-Darwinist mechanism. In chapter 6, I
will argue that many such changes are non-random, and some are self-amplifying, so
that differential survival and reproduction is in those cases irrelevant.
No matter how the mechanisms might be labeled, all of the major physicochemical
changes in the internal milieu, though initially imposed by the environment, have
been genetically assimilated, so that they persist regardless of further environmental
influence. Since genetic assimilation is especially relevant to development it is
discussed in more detail in the next chapter. Next I want to consider the buildup of
biochemical complexity in primitive organisms.
Biochemical Evolution
Biochemistry and Molecular Biology

Biochemistry used to occupy a comfortable niche between chemistry and biology.
Having discovered the general properties of enzymes, and unraveled the metabolic
pathways and the physiological actions that they governed, it broadened into
comparative biochemistry and assumed an important role in the investigation of evo-
lutionary history through comparing the primary sequences of proteins. Molecular
biology then leapfrogged traditional biochemistry to emphasize the informational
aspects of macromolecules. It has broad, practical applications in medicine and
agriculture, as well as major theoretical implications for evolutionary biology, and a
hybrid vigor derived from the cross-fertilization of physics, virology, bacteriology, and
genetics. For better or for worse it has also come to dominate traditional organismal
biology.
Yet, as an erstwhile evolutionary physiologist and a comparative enzymologist, I
find traditional biochemistry as pertinent to the larger issues of evolutionary history
as molecular biology. The genes, when permitted, dictate the amino acid sequences of
the structural proteins, enzymes, and hormones. These products contribute to form,
and do the work of the organism, and they cooperate in an organizational hierarchy
that transcends molecular properties. Molecular biologists are beginning to realize this
to the extent that they declare that now they have tidied up the human genome
project they will apply all their resources to the study of proteinsfrom genomics
to proteomicsa step in the right direction, but something that biochemists were
already doing a quarter of a century ago, before they were so rudely interrupted.
Physiologists have always had a pragmatic attitude to reduction as a methodology.
Analysis at the molecular level simplifies matters and allows the identification of
significant functional and evolutionary features that also relate to the whole
organism, which is the true value of reduction in the first place. However, molecular
functions should not be allowed to become intolerant abstractions, as Woodger
called them.28 A gene is an intolerant abstraction if its molecular structure is worked
out but its interactions and differential expression in the organism are ignored.
Reduction with an ism attached is often intolerant methodology. Some biochemists
and molecular biologists declare Im a reductionist, and proud of it, and do not seem
to mind that their graduate students, when asked what their molecules come from,
answer the Sigma Catalogue.
That said, the genome is a dynamic structure with upward causal effects on the
organism as well as being subject to change from downwardly acting causes. Molecular
biology has a great deal to contribute to the principles that I have been establishing in
this chapter. For instance, although I excluded population variability from the
definition of adaptability, there are plenty of examples of adaptability at the genome
level. And for the sake of clarity, their examination at this level is necessary, not
forgetting that the behavior of genes, transposable elements, histone-binding, and
methylation are affected by the environment of the cell, the organism at large, and the
external environment.
Biochemical Origins and Complexification

Life proverbially began in the primeval ooze, and trying to understand how it emerged
is like being thrown in at the deep end of the swamp. It would be simpler to get on
with a discussion of biochemical evolution at the point where recognizable
prokaryotes were in place. But the origin of life is the first great biological emergence,
in other words the all-or-nothing appearance of a living entity from the inanimate
without the participation of natural selection as formally defined. If the origin of life
cannot be left out, how can enough momentum be built in the mental mud to
advance our understanding of it? We can try to study model systems logically, but the
rest is largely speculation that does not get us very far. And when you listen to what
some of the authorities on the subject are saying, they are obviously swimming in
158 Chapter 4
ooze as well, with little more in common than mutual disdain. So there is not much
to lose in trying for some coherence and consistency by our own intuitive efforts.29
Organic macromolecules emerged from abiotic substrates before anything like an
organized cell existed. What those substrates were, and where on Earth they occurred
are two of the controversial questions, and answers have ranged from shallow water,
benthic marine clays, to deep rocky fissures around hydrothermal vents. Some of the
most ancient prokaryotes still live under pressures and at high temperatures that used
to be thought incompatible with survival. Other solutions, focusing on extraterrestrial
origins, have suggested the slush of comets that passed near the sun, and some
suggestive data have been acquired from experiments that attempt to recreate deep
space conditions.30 Since it is conceivable that life originated several times, both on
Earth and on Mars, before its life-support conditions deteriorated, it is not out of the
question that each planet was seeded by spores from the other, contained in material
blasted off by bolide impacts, and that Earthly (or Tellurian) life could have been
finally extinguished on Mars, while Martian life lived on to become us on Earth.31 But
once biological macromolecules made their appearance in cell-like complexes, most of
their remaining evolution, and the extension of primitive autocatalyzing
metabolisms, has been organismal.
How the biochemical complexity of primitive eukaryotes emerged is partly
answered by the endosymbiosis theory discussed in the previous chapter. But how did
the molecular complexity of the earliest proto-prokaryotes evolve? Herman Mullers
naked gene hypothesis, based on the model of viruses that contain only protein and
nucleic acids, was one of the earliest reductionist explanations. But all viruses require
a living host cell for their reproduction; as degenerate cell products they are worthless
as models for primitive life forms. Nevertheless, variants of the naked gene idea has
persisted among molecular biologists.
Nucleic acid polymers, randomly and abiotically synthesized in the primeval dilute
soup, could have adsorbed amino acids, in a coherent order, according to their degree
of attraction to the nucleic acid bases. But unless the abiotic polynucleotides also had
an enzymatic ligase functionan ability to link amino acidsthis would be unlikely
to have resulted in the spontaneous polymerization of proteins. Nevertheless
randomly generated free nucleotides and amino acids could have been brought into
close physical association by clay adsorption, or in heterogeneous coacervates, and
being in the same place at the same time is a necessary condition for the generation of
more intimate interactions and symbioses out of loose associations. Von Neumanns
1966 theory of self-reproducing automata, well known among science-fiction
enthusiasts, has slowly been invading biology. It proposes that the minimum require-
ments are a blueprint, a constructor, a replicator, a switch that activates the copying
process, and a box that keeps the bits close enough together to interact, but as an open
system. Living processes require the metabolic association of molecules that can access
a source of raw materials, and can self-replicate faithfully. But what came first?
The primary emergent feature of DNA is its ability to be copiedprovided the full
resources of a cellular unit are present. Self-copying is bifunctional, in the sense that
an entity that reproduces also survives in its offspring, even in destabilizing
conditions. Highly stable polymers, such as plastics, can survive much longer than
vulnerable nucleic acids or proteins. But to achieve a reasonably faithful copy a living
system has to be unstable enough to come apart and go back together again, making
it vulnerable to physicochemical influences, error-prone, and thus raw material for
natural experiments.
Early molecular biologists used the expression the central dogma for the assertion
that information for synthesis can only flow from DNA to protein, despite the already
well-known fact that some viruses consist of only RNA and protein. RNA viruses can
synthesize DNA using the enzyme reverse transcriptase. Not surprisingly, RNA, of a
molecular type similar to messenger RNA, a long-stranded molecule with a genetic
code in its primary structure, is now the most popular candidate as the primordial
gene.32 But to copy itself, or to make both DNA and protein, RNA would require
ancillary support. A more appealing model is an RNA that has a catalytic, or enzyme-
like function, like that of ribozyme. Genetic engineering of this enzymatic RNA has
produced forms that polymerize RNA, and some that break peptide bonds in proteins.
Other laboratory experiments have randomly produced RNAs that can string together
new strands, using high-energy phosphates in the process. And natural experimenta-
tion might have brought about the same results at the dawn of life.
Familiar ribosomal RNA that participates in the protein synthesis found in present-
day living cells has the ability to link amino acids through peptide bonds. The
archetypal RNA could have done that, with an additional function of self-replication.
The proteins would initially have been randomly structured. These possibilities point
to what Leslie Orgel (1994) calls the RNA world, from which emerged the last
common ancestor of all subsequent living organisms. Another option would be a
protein world where pre-existing catalytic proteins acted as templates that attracted
and polymerized nucleotides or simple bases. Thus, a molecule that already had the
spontaneous function of aligning nucleotides could have also been able, indirectly, to
replicate itself. Such simple systems could have kept up with entropic wear and tear of
their organized complexity, and some of the randomly structured proteins could
already have had functions that were meaningful for protobiont integrity.
Stuart Kauffman (1995) has taken a different tack, focusing on catalytic closure as
a property of a chemical system responsible for the emergence of life:
Each cell in your body, every free-living cell, is collectively autocatalytic. No DNA molecules
replicate nude in free-living organisms. DNA replicates only as part of a complex of collectively
autocatalytic network of reactions and enzymes in cells. The cell is a whole, mysterious in its
origins perhaps, but not mystical. Except for food molecules every molecular species of which
a cell is constructed is created by catalysis of reactions, and the catalysts themselves are created
160 Chapter 4
by catalysts created by the cell. To understand the emergence of life, I claim, we must understand
the conditions that enabled the first emergence of such autocatalytic molecular systems.33
Kauffman argues from established models that as autocatalyzing systems become more
complex there emerges a self-sustaining system with a novel complexityanalogous
to a shift from the liquid state of water to solid ice. A living metabolism crystallizes.
Life emerges as a phase transition.34 Julius Rebeck and his colleagues have worked on
non-DNA/RNA self replication of synthetic molecules based on adenine ribose linked
with naphthalene.35 He suggests a model for a self-replicating coat of protein. But
these, though they show that polynucleic acids are not essential for reproduction, are
more rigid than living systems and have no means of capturing or generating energy.
Chemist Denis Schwartz has communicated to me his concept of how catalytic closure
itself might have happened as an emergent phase shift. He has modeled a pre-RNA
autocatalytic, self-energizing chemical system based upon the kinds of molecules
found in redox reaction in mitochondria, and as parts of the nitrogenous bases in
nucleic acids (adenine again). It bends no physical laws and can probably be tested in
the laboratory to determine the limiting conditions of its generation. Moreover, it is a
versatile or metabolically multifunctional system that is self-organizing in space and
timemuch more so than the RNA world. Schwartz believes that the catalytic
potential of ribozymes is too small for them to be candidates as ur-molecules. But his
system could generate RNA and its own lipid membranes. As to the time frame for the
chemical emergence of such a system once the generative molecules had been
accumulated, I asked Seconds or eons? Minutes, maybe years, he replied.36 Thus,
both ribozymes and protein enzymes could have been consequences of a Schwartzian
abiotic generative complex contained in protobionts. Think of the latter as primitive
units that have a membrane-bound, heterogeneous chemical structure, but cannot
reproduce themselves except by random fission. They were open system/dissipative
structures that concentrated the more generative autocatalyzing chemicals, allowed
crude reproduction as a first step toward the emergence of a living cell. Randomly
generated proteins and ribozymes could have been capable of weakly catalyzing
multiple reactions, instead of having the single specific reactive properties of familiar
enzymes. This would have increased the probability of spontaneous emergence of a
self-sustaining system that could continue to feed on other chemicals in solution in
the environment, more life-like in the sense of faithful reproduction. Like Kauffman,
Schwartz argues that the emergence of life was inevitable, given the presence of a
simple chemical precursor system. And it was fast.
The biologist A. I. Oparin used colloidal clumps of coacervates as models of
protobionts in his pioneering experiments, reviewed in English in 1938. Coacervates
grow by absorbing molecules from solution; they crudely reproduce by disintegration
and further absorption, and they can be designed to absorb energy and release it for
biochemical reactions, an important step in sustaining a reliable synthetic ability.
Proteins that were finally polymerized in a protobiont would have to have shared
compatible physical characteristics, so that they could co-exist in an aqueous microen-
vironment of a particular hydrogen ion concentration, electrical potential, and
electrolyte composition without disintegrating or cross-bonding irreversibly.37
Polymerization of proteins and nucleic acids had to go on fast enough to keep up with
their rate of degradation. But the necessary high-energy molecules were already
present in the constellation of protobiont features. And adenosine triphosphate
remains the most common energy primer in living systems.
The formation of a simple cell membrane around coacervates is not a major
theoretical hurdle, since bipolar molecules such as phospholipids, if mixed with water,
tend to orientate themselves as monolayers at the surface If they are stirred, they sort
themselves spontaneously into double layers, and can associate with electrically
charged molecules like proteins. If the proteins protrude through the membrane they
can continue to act as absorbers and concentrators of molecules in solution in the
outer environmentforerunners of diffusion channels, ion pumps, cellular adhesion
molecules, and cell surface recognition molecules. In the early days of protobiont
formation, different types would have coalesced randomly, as well as reproducing by
fragmentation, permitting mix-and-match experiments in mainly additive complexi-
fication. These speculations do not preclude the possibility that the initial
concentration and primitive organization of the molecules that made up the
protobionts took place on a heterogeneous, adsorptive surface such as a clay, as
suggested by Graham Cairns-Smith in The Life Puzzle (1971). It might have been
harder in the aquatic pressure cooker of a thermal vent, since heat-resistant
biopolymers would be less flexible, and phospholipid membranes are unstable at high
temperatures.
Among their emergent properties, protobiotic units would inevitably have had
electrical potentials across their lipid membranes because of Donnan equilibria: dis-
proportionate ionic concentrations resulting from the presence of large, non-diffusible
ions within the membrane system. Such electropotentials created the opportunity for
membrane excitability, even before the emergence of the ion channels, and gates and
pumps that we now associate with nervous activity.
A necessary complement to the emergence of a living, complex, autocatalyzing
system is stable coordination of its components to reduce the chaos of infinite
interactive possibilities to a few predictable pathways. This requires a degree of
homeostasis that resists change, though in a living system there must always be
sufficient inherent plasticity to allow ultimately for reproduction and the evolution of
permanent change. Kauffman and his colleagues have shown that model physical
systems spontaneously assume such propertiesin the absence of any self-
reproducing qualities, and in the absence of any influence that might be equated with
natural selection.38 In his personal communication to me, Schwartz goes further, to
162 Chapter 4
describe his chemical system as one that not only emerges by autopoesis, but becomes
more complex by orthogenesis. As a chemist he finds nothing heretical about self-
amplifying systems. Integrity, survival, order and complexification are emergent
qualities of complex physicochemical systems, even in the absence of reproduction by
means of a DNA-like mechanism. But they had the potential to generate such a
mechanism.
Kauffman and Schwartz demonstrate that the emergence of ordered systems can be
rapid, and geological evidence shows that in the history of our planet life emerged just
about as soon as it was cool enough for it to do so. In all probability there were
multiple initial experiments in emergent life forms. Some were insufficiently robust to
survive environmental contingencies, and some may have pooled their resources sym-
biotically. By that time, some protobionts would have been at the chemoton stage
with a rudimentary metabolism and self-replicating coded polymer, or the
progenote stage with a rudimentary, imprecise linkage between its genotype and
phenotype.39 The progenote, in which the mechanisms of protein synthesis were still
evolving, has been proposed as the cenancester, or last common ancestor, of all
surviving organisms from Archaebacteria to humans.40 Determination of the exact
nature of that cenancester from surviving prokaryotes is difficult because of
subsequent multiple exchanges of genes between the lineages. However, when they
achieved accurate replication, available environments would have filled up, and then
competition and predation would have reduced the array of experiments, influenced
the refinement of internal coordination, and the establishment of dynamically stable
ecosystems.
As unifunctional enzymes, whose products positively affected the integrity of the
cell, emerged, along with specifically coded templates for their synthesis, they were
subject to adaptation to the local environment of the cell. Michael Conrad (1990)
suggests that the structure of protein molecules already provided a variety of buffering
mechanisms involving redundancies in the numbers of weak bonds and amino acids,
amounting to molecular homeostasis that resisted change in the cellular environment.
He also points out that other protein features could result in the amplification of small
changes, making them more evolvable.
The simplest unicells have signaling systems that pick up external stimuli, and
communicate them with the interior; they may only have two or three components.
But intercommunication with parallel pathways is sufficient to generate new
complexity. These generative conditions for signaling are greatly complexified in
nervous systems. For example, there are four major signaling pathways communicat-
ing with the post-synaptic membrane of mammalian neurons. Each pathway has
multiple components that intercommunicate with parallel pathways, making the total
number of possible combinations astronomical. This illustrates that while the
generation of complexity in terms of number of interactions is easy to appreciate, the
empirical problem is in discovering how the systems are constrained and limited to an
efficiency that is not hindered by meaningless interactions. It also illustrates that the
contingent mutual impact of independently evolved biochemical pathways has
played a role in minor saltatory emergences within simple cells. In their essay
Complexity in biological signaling systems (1999) Weng, Bhalla, and Lyengar
develop this view of biochemical complexity with a computer simulation of a
simplified four- pathway system:
Such a network exhibits interesting emergent properties, including integration of signals across
different time scales, generation of distinct outputs depending on the amplitude and duration of
the input signals, and the presence of feedback loops that behave as bistable switches to process
information flow through the network. Although this first glimpse of emergent complexity
appears to be intriguing, rapidly accumulating experimental evidence suggests that several other
considerations need to be taken into account in order to develop a minimally accurate picture of
a living cell. Prime considerations among these are compartmentalization and regional organiza-
tion of signaling components.41
These authors go on to discuss hydrophobic lipid and hydrophilic aqueous compart-

ments and the difficulty of quantifying the micro-quantities of ions therein. They also
note the importance of the cytoskeleton for anchoring membrane receptors in
position and providing scaffolding for an assembly line along which a series of
enzymes process their substrates in a well-defined sequence and with an efficiency and
specificity that are orders of magnitude higher than would be possible in freely
diffusing systems.42 MAP-kinase (= mitogen-activated-phosphorylase-kinase)
pathways exemplify this scaffolded order. The emergent property is called reaction
channeling. Even in vitro, the efficiency of the reactions and specificity of flow is
retained. Where biochemical pathways are isolated within subcellular compartments,
such as the mitochondria and nucleus, intercommunication is possible through the
diffusion of translocation molecules.
Subsequent biochemical evolution is a mixture of natural experiment and conserva-
tion. (This will be elaborated in chapter 6.) When DNA is brought into the picture, the
complications for analysis and understanding the complexities of molecular intercom-
munication are again astronomical. Compared to these problems the identification of
the genetic code and even the completion of the human genome project seem almost
simple. The code for structural proteins and enzymes is almost identical throughout
the genophores or chromosomes of all living organisms. Any mutations that cause a
frame shift in reading the code of an exon, by the deletion or insertion of a base, for
example, can throw off protein synthesis so badly as to be lethal. On the other hand
a non-synonymous point mutation in a single base, i.e., one that changes the code for
one amino acid in the primary structure of the protein, produces an alteration of
protein function that may be advantageous, neutral or detrimental. By conventional
wisdom all of the potentially beneficial variations have been tried and retained, and
164 Chapter 4
any further mutations will only repeat old mistakes, assuming that internal and
external environments remain constantbig assumption. However, Lynn Caporale
(2003) marshals a host of instances of non-random hypermutability in specific regions
of the genome that constitute gene adaptability. Though most common in
prokaryotes, these phenomena also occur in eukaryotes. The construction of
antibodies is the example that will be most familiar to her readers.
Another conservative feature of biochemical evolution is that similar spectra of
genes and proteins, structural, regulatory, and enzymatic, are found throughout the
living world. This re-emphasizes the impossibility of explaining evolutionary
divergence or progress in terms of the cumulative possession of unique proteins or
biochemical reactions. The same old genes and proteins are mix-matched time and
again to come up with modified variations and combinations.
Repetitive Differentiation
Gene amplification is a versatile process that widely affects physiological evolution.
Alteration of existing DNA removes its old function from the organisms repertoire. If
that old function was essential the mutation is detrimental, even if the modified
protein has an immediate utility. One way to get around the problem is to duplicate
genes, and leave some to carry out business as usual, while the duplicates provide the
raw material for natural experimentation. In this way biochemical systems can be
intensified, complexified, and made more adaptable. This is where repetitive differ-
entiation comes in.
E. D. Copes antique term repetitive addition referred to anatomical complexifica-
tion that resulted from segmentation in worms and arthropods. He and William
Bateson realized independently that the functional-anatomical repertoire of an animal
could be enhanced by repeating, or segmenting, some of the old parts. These could
continue doing what they always did, assuming that those functions remained
necessary, and the others could experiment with new functional morphologies.
Appendages used for swimming by the old segment could be modified for walking in
the new one, repeated nerves and muscles still working in the same basic way initially.
The potential for a particular segment or group of segments to produce some kind of
variant of a limb resides in the expression of a cluster of developmental Hox genes that
have also arisen by repetitive differentiation. But other organismal mechanisms
participate as well as the genes. In the middle of the twentieth century, several far-
sighted authors realized that the duplication of the total number of chromosomes, as
well as duplication of portions of chromosomes had a potential for evolutionary
experimentation. (See also chapters 6 and 8.) The old anatomical name, repetitive
addition, is tautological, and it does not imply differentiation as well as multiplica-
tion. The concept is filtering into comparative biochemistry and molecular biology.
And in epigenetics it has been included in the syndrome of modularity. But much has
yet to be made of it in an evolutionary context, so I dare to modify the name to

repetitive differentiation.43
The concept is very useful at the level of molecular changes, where it refers to a gene
or a specific DNA sequence that has repetitively duplicated, and whose duplicates have
then mutated into differentiated variants. These are sometimes called variant
repeats or varied repeats and the result of simple duplication without differentia-
tion is dose amplification or dose duplication. It has long been known that many
proteins exist in a variety of molecular forms with slightly different electrical
properties, allowing them to be separated by electrophoresis; in the case of catalytic
proteins they are called isoenzymes. They have functional differences in addition to
their electrophoretic ones, and can emerge through simple mutation as well as
repetitive differentiation. There may be a number of mutant allelic variants present in
a population, any two of which a given diploid individual will possess. However
repetitive differentiation provides an individual with an extensive suite of variant
repeats. One of the advantages of such a suite of isoenzymes was made clear in the
now classical example of salmon muscle kinases, enzymes that release energy for
swimming.44 The isoenzymes have different temperature optima, and switch on and
off according to the ambient temperature, so that the fish can keep on swimming
efficiently in a range of temperatures instead of slowing down when the temperature
drops, as it would if there were only a single kinase with a fixed and narrow
temperature optimum. A significant portion of amphibian genomes is taken up with
variant repeats that ensure normal development under different temperature regimes.
Repetitive DNA, amplified DNA or duplicate genes as the bits are sometimes
called, are very common, many of them, such as satellite DNA near the centromeres
and telomeres, apparently doing nothing, or at least not contributing to protein
synthesis. (But see chapter 6.)
Many enzymes come in a number of isoenzymic forms, some simply allelic variants
of non-duplicated genes, some variant repeats. Susumo Ohno (1970) observed: Only
the cistron which became redundant was able to escape from the relentless pressure of
natural selection, and by escaping, it accumulated formerly forbidden mutations to
emerge as a new gene locus.45 R. J. Britten and E. H. Davidson (1971) supported this
opinion, pointing out that repetitive DNA gives the organism the opportunity to
experiment with point mutations of the original gene, out of sight of natural
selection.46 This gets over the problem that if a gene that is doing something useful
for the organism mutates, it is no longer available for the original function, and its
substitute, while it may be more useful under certain circumstances, might be useless
if the conditions of existence revert. So adaptability can be achieved through repetitive
differentiation. Suites of mutant genes and transposable elements might be held on
standbypotentially useful if circumstances changewhile the original keeps on
doing its necessary job. These natural experiments need not interfere with the internal
166 Chapter 4
coordinative conditions of the cell or organism unless they are constitutive, i.e.,
always turned on, and wasteful of energy. Therefore internal selection favors the
refinement of feedback control. In tissues where they are not required they are
inhibited by histone binding and methylation. Plasticity in natural molecular experi-
mentation can also be achieved by both duplication and differentiation and
rearrangements of subgene portions of DNA, the exons that carry the code for the
meaningful bits, and the nonsense introns providing for the rare emergence of func-
tionally novel genes. This is dealt with more extensively below in the section New
Genes for Old. It should be mentioned here that changes in methylation, acetylation,
and histone binding patterns that repress gene expression can be environmentally
induced, and the impact transmitted from generation to generation, as Eva Jablonka
and Marion Lamb pointed out in Epigenetic Inheritance and Evolution: The Lamarckian
Dimension (1994). This has now become acceptable to some mainstream molecular
biologists, who are now speculating about the non-DNA inheritance of acquired char-
acteristics.47 The concept of repetitive differentiation simplifies the problem of how
metabolic pathways evolved. In the ancient, anoxic, aquatic environment of Earth
many organic molecules were synthesized abiogenically by the energies of solar
radiation, volcanic emissions, electrical discharges, and impacts of bolidesthe
general term for meteors, comets, asteroids and other space debris that impact Earth.
The first protocells, with a simple biochemistry, and unable to photosynthesize,
depended on abiogenic food molecules in their environment for energy, growth, and
reproduction. What happened when the abiotic energies diminished and the
oxygenation of the environment began to destroy free organic molecules faster than
they were made?
One way to make up the loss was to prey upon other organisms that already had
essential compounds. Another was to alter precursors that were still available. The
enzyme that makes a particular product might be duplicated and differentiated to
become one that can convert the first product to something else. Substrate structure is
already related to product structure, thus the active sites of enzymes in a metabolic
pathway tend to be similar as well. Therefore it is conceivable that some of the
enzymes in a given pathway arose from a single original gene by repetitive differenti-
ation. But there remains the problem of how the evolutionary process could respond
quickly enoughwhen the abiotic source of essential molecules was depleted, the
final phase would have been sudden, and drastic. It only takes a month or so for an
oceanic phytoplankton bloom to crash because it has used up key mineral nutrients,
usually phosphate. The random evolution of a series of enzymes, one at a time, by
repetitive differentiation, could not have responded in such a timeframeduplica-
tions and mutations are instantaneous, but are not made to order. Instead, some
biochemically adventurous cells had to have had a pre-existent suite of enzymes,
immediately able to make good the deficiencies.
B. E. Wright (2000) proposes that biosynthetic pathways evolve as a result of

depletion and interconversion of related metabolites. Starvation may result in the
absence of a key transcriptional inhibitor metabolite. Subsequently, loss of feedback
control is followed by transcriptional derepression of specific enzyme-encoding genes.
Given that increased transcription is linked to higher rates of non-transcribed strand
mutation, this chain of events would give rise to an increased number of variants that
might initiate novel catabolic pathways, enabling the derepressed enzyme to utilize a
new substrate. Experimental evidence demonstrates that this type of biochemical
evolution is not uncommon, and Wright believes that mutation is not exclusively
random, and that the environment plays a significant role in evolution at the
molecular level. Simple but biochemically versatile prokaryotes could also acquire
additional DNA through transformation, conjugation, and transduction, and such
cells could also have provided the foundation of a food pyramid.
Before eukaryotes emerged, the elaboration of membrane proteins was well under
way. These variously responded to extracellular influences by recognizing external
stimuli and absorbing specific nutrients. With the advent of multicellularity their
influence was extended for cellular communication. Some of the most complicated
examples of repetitive differentiation are to be found in the neural and hormonal
systems of multicellular animals. Ion channel proteins for potassium, sodium, and
calcium involved in selective activation of impulses in nerve cells evolved by repetitive
differentiation. Hormones that affect water transfer across cell membranes mostly
belong to the same peptide family. For example, vasopressin, the antidiuretic hormone
of mammals that causes urine retention, increases the water permeability of part of the
kidney tubules. It is closely related to the molecule that makes frogs absorb salt from
the environment, and one in freshwater fish that causes increased urination rather
than water retention.
Prolactin stimulates lactation in mammals, causes broodiness and crop milk
production in birds, and acts as a growth hormone in reptiles. It may have been
involved in alterations in gill membrane permeability in primitive fish, and it reduces
salt secretion from the gills of modern bony fish. Prolactin is also found in inverte-
brates. Most of its functions have to do with the transfer of solutes and water through
membranes by altering porosity; so major reconstruction is not needed to switch high
permeability over to low permeability. Prolactin is itself a derivative, through
repetitive differentiation, of the more ancient molecular family of growth hormones.
Their genes too have undergone rapid episodes of duplication and variation
throughout vertebrate evolutionary history. Among the mammals, alteration of
growth hormones coincided with sustained bursts of rapid evolution in the
artiodactyl and primate lines.48 In humans, three variants are involved in placental
function, in addition to the ancestral growth hormone gene.49
168 Chapter 4
Hormone-like steroids and peptides are ancient molecules found in prokaryotes.

Mammalian subjects have been intensively investigated because of medical priorities
in physiology. The gaps in our knowledge of their functional evolution from bacteria
to vertebrates simply reflects a relative lack of interest in other animal groups.
However, there is some consensus that a few major events catalyzed vertebrate
evolution. The duplication and reduplication of the entire vertebrate genome in the
late Cambrian quadrupled the potential for adaptability of the entire lineage through
natural experiments in differentiation of the repeated genes. Not only were novel
variations of the existent possible, but new major systems, such as the immune system
emerged. Furthermore, early in the craniate line, the neural crest emerged as a source
of cells that were to be fundamental tools of vertebrate evolution. This improvement
in functional anatomical evolvability is a story for a later chapter on developmental
evolution. However, it is a matter of historical record that embryonic innovations
together with physiological adaptability permitted our aquatic ancestors to survive the
major catastrophes that terminated the Ordovician and Devonian, and, once on land,
to soldier on through the Permian, Jurassic, Triassic, and Cretaceous extinctions. There
was a lot more to it than being in the right place at the right time.
Comparative studies have begun to establish hormone lineages both in the
protostome and deuterostome lines of animal evolution. Many of them are mediated
by ubiquitous second messengers, such as calcium ions, and cyclic adenosine
monophosphate (cAMP). The latter is a close relative of adenosine triphosphate (ATP),
which universally energizes biochemical reactions. It is also related to the nucleotide
constituent of DNA that contains the base adenine. Among the many processes
activated by cAMP are the hormonal control of intestinal activity, blood sugar, urine
volume, blood calcium levels, reproduction, and the production of a variety of neuro-
transmitters. It also has an inhibitory effect on other hormonal actions.
The question of how a single mediator can elicit such a range of responses, and
which of them are effected in specific tissues, is again addressed by the concept of
repetitive differentiation. The membranes of differentiated cells are responsive only to
specific hormones, although they mostly possess an enzyme, adenylate cyclase,
involved in the conversion of Mg-ATP to cAMP. Then, when cyclic AMP is produced,
there are specific, differentiated enzymatic response mechanisms that again are char-
acteristic of the cell type. The ability to synthesize cAMP remains a general feature of
many different cells, but its production and action depends on repetitive differentia-
tion of cell receptor and effector molecules. A final point relating to homeostasis is
that in mediation processes involving hormones and series of enzymes there can be a
cascading amplification of the products, and control by rapid enzymatic degradation
of the activating hormones is necessary. The dangers of unregulated positive feedback
mechanisms are common in myth. The Fantasia version of The Sorcerers Apprentice,
may strike a chordMickey Mouse tries to stop the magic broom from inundating the
alchemists laboratory; but when he duplicates it by chopping it up, the cascade is

amplified.
New Genes from Old

The most elementary knowledge of DNA action ought to dissuade anyone from the
old notion that new physiological abilities are due to the acquisition of brand-new
enzymes. The complexity of a protein requires the coded complexity of DNA, which
cannot pop into existence out of nowhere. Classical examples of protein novelty
keep being eliminated. Prolactin is derived from the older growth hormone family.
Hemoglobin is a protein that appears to have evolved de novo a number of times. But
every mitochondrion has the iron-porphyrin heme that makes hemoglobin interact
reversibly with oxygen, and suitable globin proteins are universally distributed. Prior
to the emergence of hemoglobin, an ancestral globin gene lost an intron and then
duplicated. At some time in the late Pre-Cambrian the duplicates mutated, and from
the divergent coding emerged both myoglobin (the oxygen carrier of muscle cells) and
hemoglobin (which is usually found in blood). Further gene duplication provided for
the emergence of the hemoglobin supermolecule. Sequencing evidence shows that
when the original duplication occurred that gave the hemoglobin molecule its two
globin strands there was an increase in the rate of base substitutions in the duplicate
genes.50 Functions can be modified or even changed by repetitive differentiation. For
example, there are suites of hemoglobins that function under different physiological
conditions in individual organisms. Adult human hemoglobin oxygenates and
releases oxygen at higher levels of environmental oxygen than does fetal hemoglobin.
Hemoglobin consists of the conservative iron-containing heme that actually captures
the oxygen, and two globin strands that modulate the action of the heme, and the
genes for the globins are on different chromosomes. This complements the hypothesis
that where there is a duplicate there is greater freedom for natural experiment. The
improved adaptability conferred by the new configuration also relaxed the strictures
of adaptation.
Another example of emergent novelty arising from repetitive differentiation is the
protein thrombin, which promotes blood clotting in higher animals. Its gene is a
variant repeat of the more ancient gene for the protein-digesting enzyme trypsin
found in digestive systems throughout the animal kingdom. Receptors for numerous
hormones involved in the regulation of digestion and blood sugar also belong to the
same G-protein-linked molecular family.51 In other words, repetitive differentiation of
genes can generate developmental and physiological plasticity.
Novel digestive enzymes such as chymotrypsin and pepsin were produced by
repetitive differentiation of the genes for trypsin and cathepsin D respectively.
Cathepsins are universally distributed in eukaryote lysosomesorganelles that have
an intracellular digestive function in invertebrates and unicells. In arthropods and
170 Chapter 4
mollusks they have been seconded as supplementary extracellular digestive enzymes

too. Cathepsins recycle cellular components during development and starvation in
vertebrates. For example, their activity is elevated in the tails of tadpoles during meta-
morphosis, and in the muscles of migrating salmon, whose protein is sacrificed for
energy and for re-investment in eggs and sperm. Cathepsins have other biochemical
roles as well; one is used to activate a thyroxine precursor.
Another protein novelty is a component of snake toxin derived from a common
molecular ancestor of pancreatic trypsin inhibitor of mammals.52 Ancient intracellular
fibrous proteins differentiated into the keratin of skin, scales, feathers, and the mucus
of hagfish. Tubulins were put to use for a variety of mechanical functions including
the contraction of muscles. An equally interesting emergence of a physiological
innovation at the gene level involves both repetitive differentiation and contingent
association of the functional domains of previously unrelated proteins. The milk-sugar
synthesizing enzyme lactose synthetase has two sequences, one derived from
galactosyl transferase, itself an enzyme of the Golgi apparatus, the other arising from
milk protein lactalbumin, which in turn differentiated through mutation of a
duplicate of the gene for lysozyme.53 Lysozyme is an ancient enzyme that protects
against some bacteria, as Fleming and Allison discovered in the early years of
antibiotics research. They first found it in human tears, but it turned out to be almost
universal.53 Lysozyme has been involved in the evolution of cellulose digestion in
mammals, as well as production of lactose. Variant repeats make the mature organism
more adaptable in changing environments.
Exon duplication, shuffling, and transposition is responsible for the buildup of
proteins involved in blood clotting in vertebrates. But a different kind of novelty is
illustrated by the crystallins of eye lenses in many animals. All that is required of these
proteins is that they be small enough to avoid clumping and be transparent in
aqueous solution. These are common properties of a wide variety of enzymes that have
been independently recruited as crystallins for the eyes of different animalsan
opportunistic molecular convergence.54 Crystallins are all coded by so-called house-
keeping genes that need to be constantly available for the production of intermediate
metabolic enzymes in most cells.
One fascinating example of a new enzyme function arising from a simple point
mutation is a change from an insect carboxylesterase to an organophosphorus
hydrolase. This confers resistance to certain insecticides. The mutation results in an
amino acid substitution that bonds with a water molecule to alter the tertiary structure
and function of the enzyme.55 The relative paucity of examples of such novel genes is
probably due to lack of investigation, but no matter how strongly selection pressure
demands that something ought to be there, it is not always forthcoming. Since lots
of people die of amino acid deficiency without having children, there must be a
strong selection pressure for a gene for protein storage. Yet most animals cannot
physiologically store protein at times of plenty, and release essential amino acids from
that store in times of famine. They can only recycle proteins that are in use as muscles
and enzymes, to the detriment of normal function. Simple molecules like glucose can
be stored as glycogen, and fat can be stored in adipose tissue. But because a particular
protein requires a correspondingly coded segment of DNA, there is an information
barrier. Amino acids cannot simply be thrown together randomly to make proteins,
and genes for protein storage cannot operate without a full complement of the amino
acids that the proteins contain. Evolution has no ability to predict what amino acids
are going to be available, nor in what erratic combinations, in the future.
On the other hand, it would be useful if our lipid deposits were more like egg yolks,
with vitelline storage proteins as well as fat. Insects seem to have pulled it off: their
fat body, which occupies much of the abdominal cavity, contains storage protein. In
some insects this is complemented by symbiotic bacteria that can turn excretory uric
acid into useable amino acids. In actuality, every cell of our bodies, including the
adipose tissue, has genes that code for vitelline protein; they would just have to be
switched on. But no amount of selection pressure has done that to compensate for
dietary deficiencies in mature vertebrates.
All the same, protein starvation in humans is often more of a political or agricultural
problem than a biological one, and that is true of other nutritional deficiency diseases.
The mammals abilities to synthesize vitamins, essential fats and essential amino acids
have regressed during its evolution, and if an adequate natural diet is available they
do not need to be synthesized. But humans put each other in concentration camps,
and used to send emissaries on prolonged sea voyages on a diet of hardtack and salt
pork. Selection pressure should not be expected to compensate for such bizarre
behavior, even for those who treat it as a real agent of evolution.
New Physiological Systems from Old

Interactions between previously independent genes and protein domains are common
evolutionary experiments. Such changes occasionally happen at the physiological
organ-system level. For example, after a period of development in the ocean, the blue
swimming crab Callinectes sapidus, enters the brackish water of Chesapeake Bay,
exposing itself to dilution physiogenesis. It responds by reducing the osmotic pressure
of its cells through the metabolism of amino acids, releasing ammonia as an end
product. Ammonium ions are then excreted into the environment in exchange for
sodium and chloride uptake. Another advantage is contingent upon this osmoregula-
tion mechanism. The oxygen-binding capacity of the crustacean blood pigment,
hemocyanin, is diminished by dilution, creating a potential respiratory problem, since
the crabs swim constantly during their migration, and need more oxygen than usual.
But conversion of ammonia to ammonium ions increases the blood pH, which coin-
cidentally makes the hemocyanin more efficient.56 This congruity of previously
172 Chapter 4
unrelated functions represents emergent adaptabilitythe whole is greater than the

sum of its partsbut it is independent of homeostasis. Fish did not need such a stroke
of luck since their hemoglobin function is not diminished by dilution. A more
common example in the vertebrates is the interaction of the ventilation system with
locomotion.
Switching Biochemical Pathways

Once a functional series of biochemical reactions is in place and all of the possible
improvements have been incorporated, enzyme pathways tend to be conservative; but
they can still be altered. First, an alternative branch might be grown, whose initiating
enzyme, again originating by repetitive differentiation, competes with one of the old
ones for a common substrate. The adaptability of switching backward and forward
from the old to the new pathway is sometimes triggered by an environmental change.
For example, in facultative anaerobic respiration an animal has two choices. ATP can
be produced by simple glycolysis, in the absence of oxygen, or by using the normal
oxygen-demanding mitochondrial pathways of oxidative phosphorylation when
oxygen is available. In intertidal clams the normal response to the ebb of the tide is to
close the valves and switch to anaerobic respiration. The burrow water stagnates
rapidly and there would be nothing gained by circulating it over the gills. Glycolysis,
which is the processing of glucose to release its energy in the form of high-energy ATP
and reduced redox molecules, produces phosphoenolpyruvate.
Here the metabolic pathways branch. When the bivalve is clammed up, the pH
drops, because carbon dioxide accumulates. Greater acidity favors the action of phos-
phoenolpyruvate kinase, and initiates the full anaerobic chain of reactions.57 When
the tide comes in, the bivalve extends its siphons hydraulically and squirts stagnant
mantle water into the air. These celebratory fountains are typical of a clam beach at
the early flood; hence the saying happy as a clam when the tide is in. Accumulated
carbon dioxide is voided, and fresh air comes down the siphons. The rise in mantle
pH turns the phosphoenolpyruvate over once more to pyruvate kinase, and the
aerobic pathway is restored. As the tide ebbs, the changed environment effects a
behavioral change in the clam, and a physiological alteration of the intermediate
metabolism. Some upper shore bivalves simplify matters by using the mantle cavity as
a kind of lung when the tide is out.
In plants, a parallel switch in the pathways of intermediate metabolism has allowed
certain C3 plants to survive in dry environments. C4 plants must keep their
stomata open to obtain enough carbon dioxide for photosynthesis, thus risking tran-
spirational water loss. The C3 plants use a carbon-fixing pathway that operates at low
carbon dioxide levels, and the stomata can be closed. The difference can be seen dra-
matically in the prevalence of C3 couch grass on unwatered lawns that were originally
seeded with thirsty C4 grasses.
Regression
I have already touched upon how complex organismal homeostatic systems can
regress in a way that increases available energymostly having to do with temp-
erature homeostasis, as in the camel, the naked mole rat, and the Arctic cormorant.
The principle applies at the biochemical level too. A conservative pathway can be
circumvented simply by dumping some or all of it. As Jakob von Uexkll remarked,
the pianoforte can still bring forth complex concerti if it has lost some of its keys.
French physiologist Andr Lwoff, writing in 1944, emphasized the importance of
regression in biochemical evolution. He saw it to be parallel with paedomorphosis, the
process of simplifying the life cycle by reverting back to the form and functions of the
earlier stages. The example of a branching metabolic pathway, one of whose branches
has regressed by epigenetic suppression, or by the lability of the non-essential DNA,
illustrates his point. The pathway goes back to an earlier substrate stage where it can
take off in a different direction. This process of drawing back in order to make an evo-
lutionary leap in a different direction will be expanded upon in chapter 5.
Biochemical regression has been important in the evolution of certain modes of
excretion of nitrogenous waste. Animals that have urea as an excretory end product
have lost the ability to synthesize the urease that can break urea back down to
ammonia. Those that have uric acid as the waste molecule have lost the enzymes
uricase and arginase, the latter a necessary agent in the production of urea. Like Caesar
burning his boats when he crossed the Rubicon, these organisms have committed
themselves entirely to the new excretory venture. In the case of uricotelic animals like
reptiles, birds and land snails, the egg must accumulate nitrogenous waste, and uric
acid is the least toxic molecule. Metabolic errors that would produce urea, or worse,
ammonia, are a liability, and it is safer to get rid of them altogether. Nevertheless some
reptiles retained maximum adaptability: crocodiles can excrete ammonia or uric acid,
and aquatic turtles can excrete uric acid or urea.
Primitive nitrogen cycles have a wonderful complexity. Early eukaryotes could
probably synthesize urea and uric acid and break them back down again to ammonia.
But that was before those molecules had anything to do with excretion. Uric acid was
then part of a recycling mechanism in purine metabolism, which also involves
guanine, cytosine and uracil, some of the nitrogenous bases of nucleic acids
fundamental to cellular physiology. Urea may have been used as a temporary store of
nitrogen, and then co-opted for osmoregulation, in the way that modern marine
sharks and rays and coelacanths do, in order to maintain a low body fluid salinity
without incurring osmotic imbalance. The regression of this primitively useful
flexibility can be understood in cases like uric acid storing eggs; any other nitrogenous
waste would rapidly accumulate to toxic levels. Natural selection has no interest in
holding on to an adaptable system of low fitness when a specialized one presents itself.
The loss of uricase in humans seems like gross carelessness, since it inflicts gout, a
174 Chapter 4
painful buildup of uric acid crystals in the joints. But hyperuricemia may also have
been an epigenetic condition of rapid brain growth in the higher primates, and in
humans in particular.
Endosymbiotic Biochemistry
The ultimate biochemical complexification is found in the symbiotic coming together
of complementary systems that have already been established in independent
organismsthe acquisition of heritable metabolisms. Particulars of this kind of
biochemical emergence were discussed in some detail in the previous chapter. The
impact of eukaryotic endosymbiosis on cellular biochemistry may be seen by scanning
any textbook with metabolic diagrams that have two compartments representing the
cytosol and the mitochondrial protoplasm, with a mitochondrial membrane in the
middle and arrows going back and forth between the two compartments to indicate
the exchange of metabolites. Since the establishment of endosymbiosis there have
been many shifts of mitochondrial genes to the nucleus, and exchanges of enzymes
and biochemical reactions between cytoplasm and mitochondria. The parts have been
tuned to make up a more harmonious whole.
The energy-hungry homeostasis of higher animals is fueled by high-energy
molecules synthesized by the mitochondria. The dependable delivery of oxygen to
them resulted from the evolution of gills and lungs. In the mitochondria, oxygen acts
as the terminal acceptor of hydrogen protons and electrons from reduced carbon
molecules. Although most people associate the word respiration with breathing or
ventilation, this is only the preliminary to the absorption of oxygen through
respiratory surfaces, the transportation of oxygen by hemoglobin in red blood cells,
and the release of oxygen to the cells that need it for mitochondrial function.
Reduced carbon molecules, such as sugar, amino acids, and fats, are acquired by
animals as food, often in complex forms like proteins and starches. The evolution of
feeding mechanisms and digestive and absorption mechanisms has channeled such
fuels to cells where they are oxidized for ATP production. Nutrients largely arise from
the primary trophic level of the food chain, where the reduced carbon energy comes
largely from the capture of sunlight for photosynthesis. Therefore it is tempting to
believe that this biological primary production emerged before the evolution of het-
erotrophy, i.e., feeding on preformed organic molecules. However, the primitive
environment was probably rich in reduced carbon molecules that were continuously,
abiogenically synthesized, and the most parsimonious evolutionary interpretation is
that heterotrophy preceded chemosynthetic and photosynthetic autotrophy.
Photolysis, the breakdown of water into hydrogen and oxygen by light, is a
spontaneous abiogenic process too, and any hopeful prokaryote that could use
hydrogen to reduce carbon dioxide, as some of the earliest Archaebacteria did, could
have enjoyed simultaneous environmental expansion and energetic independence by
harnessing water photolysis with a chlorophyll-like molecule. One hypothesis

suggests that chlorophyll originated in organisms that used infrared energy rather
than light for hydrolysis.58
Photosynthesizing prokaryotes were eventually acquired along with protomito-
chondria to make independent phytoplanktonic eukaryotes. Not only were these cells
able to live in diverse aerobic and anaerobic conditions, they turned the dangerous by-
product, oxygen, into an energetic asset, although sometimes energy was bled off as
bioluminescence. They were also in a position to survive the inevitable consequence
of their own biochemical adaptability, namely the oxygenation of the ancient anoxic
environment, and the creation of a new biosphere, within which oxygen-breathing
organisms might evolve. In the longer term this made it possible to achieve the high
metabolic rates required for the development of complex nervous systems. Plants
created the conditions for the emergence of creatures that could initially browse on
themand eventually think about their role in evolution.
The evolutionary history of physiology involves biospheric changes caused by
organisms, and changes in their internal milieux caused by the environment. These
were intensified as greater adaptability permitted more flexible behavior and
exploration of more extreme conditions. We need to look at ecological conditions
where natural experiments can prepare for emergence into new environments, such as
interfaces between oxygenated and anoxic regions, between sea water and fresh water,
and between aquatic and terrestrial. During the course of evolutionary history, envi-
ronments free from competition and predation, rich in food resources but rife with
physiogenic challenges, awaited the physiologically and behaviorally adventurous.
Rapid diversification could occur until the climaxes of dynamic stability were reached.
In the past there were also environments swept clear by catastrophes. Mass
extinctions, drastic disruption of food sources, instantaneous changes in temperature,
and lingering climatic change, affect every arena of evolutionary causation.
Competition, and predation may be removed entirely, and physiological adaptability
is immediately at a premium for simple survival. That adaptability has evolved in part
through progressive improvements in regulatory systems that stabilize the internal
milieu, and let the organism live la vie libre.
Physiology, Developmental Biology, and Evolution
I remarked earlier that the physiology of the mature organism has to be studied in its
own right rather than as an extension of developmental physiology. Yet it should
already be obvious that changes in the interactions between mature organismal
physiology and developmental processes are crucial. Therefore, in anticipation of the
following chapter on development, a few general remarks about the links between the
physiological, behavioral and developmental arenas might be useful.
176 Chapter 4
Roy Pearsons synthesis of the physiological qualities of the developing and mature
organism is a good start. He also places it in an environmental context: . . . the
common thread woven through the problems of macroevolution, morphogenesis and
cancer is the hormonal-homeostatic complex of the organism. Life history
(environment) interlaces with homeostatic and thus homeodynamic forces to create
the organisms evolution, development and demise.59 Pearson argues that if adaptable
responses to new environments have an endocrinal basis, the new environments can
affect development and reproduction. The vertebrate hypothalamic/pituitary/
thyroidal/adrenal/gonadal axis which regulates homeostasis is also intimately
involved in metamorphosis (development) and reproduction (e.g., vitellogenesis and
spermatogenesis).60
Eventually, in animal evolution, many epigenetic responses to environment are
genetically assimilated. After birth, human babies do not have to be made to stand up
and manipulate objects in order to acquire a typical human gross anatomy. That
process is already under way in the fetus. Yet bipedalism requires a mechanical striving
during childhood, so that there is an ontogenic adjustment of the skeleton and
musculature. Brain development also requires ontogenic experience, particularly in
learning, to bring out certain potentials. The idea of the genetic internalization of
environmental effects was pursued by Schmalhausen, who called it autonomization.
It is common knowledge that reproductive physiology and behavior, as well as
dormancy and other physiological factors in plants and animals are often governed by
climate and season. External physical stimuli act through hormones or neurosecre-
tions to influence the genes responsible for synthesizing the other proteins
appropriate to the season. Schmalhausen was sure that primitively the environment
was a major inducer of developmental change, and that gradually the induction was
internalized, thus complementing Bernards precept that independence from external
change was the precondition of physiological freedom. Schmalhausens stabilizing
selection included internal co-adaptations that would lead to physiological stability,
or homeostasis. As part of the process, duplicative mutations of simple regulatory
mechanisms could build up an array large enough to take over from the old environ-
mentally induced onean evolutionary hypothesis equivalent to the concept of
repetitive differentiation.61 Finally, disequilibrating influences of stressful environ-
ments might be needed to induce evolutionary changes to occur, and to escape from
stasis.
Epigenetic modification can be initiated by changes in temperature, precipitation,
photoperiod, food (or lack of it), and population density, as well as extrinsic biological
triggers like pheromones. The morphological, physiological and behavioral conse-
quences seen after metamorphoses are particularly striking. Digestive, locomotory and
respiratory systems may be totally reorganized for example. Locusts start out as simple
grasshoppers and do not form their devastating flying swarms until an accumulation
of environmental factors trigger changes in adult morphology, physiology and

behavior.62 Another discovery of how overcrowding affects these factors is the
appearance of monstrous carnivores in salamander populations.63 Mary Jane West-
Eberhards Developmental Plasticity And Evolution (2003) is the best current source for
these kinds of cases.
Conclusions
Referring back to the checklist of questions in chapter 2, which were to be kept in

mind by explorers of emergent evolution:
1. Molecular and functional-morphological repetitive differentiation is common to

the arenas of association, and physiology. As we work through the next chapter we
will see that repetitive differentiation at the gene, cell and organ levels are important
components of developmental differentiation. Furthermore there will be commonali-
ties found between disequilibration of existing homeostatic stabilities and
homeorhetic stabilities as part of emergent evolution.
2. The generative conditions from which physiological emergences spring combine

physiological and behavioral adaptability with environmental opportunity at
interfaces between ecosystems. Concentration at interfaces is also relevant to the
origin of protobionts and to endosymbiosis.
3. Novel emergent qualities of physiology, especially those with a symbiotic content,

altered external environments, so that a way was prepared for further natural
experiments and ventures
4. Transition to new environments caused disequilibrating physiogenic change that

became a key generative condition for further modifications. In higher animals the
acquisition of a sophisticated homeostasis potentiated novel behaviors and
anatomical specializations.
5. The interaction between organism and environment vindicate the neo-Lamarckist

argument that the environment imposes change, and Lamarcks law that the organism
responds to its environment. These are important evolutionary factors, even in the
absence of a somatogenic mechanism to genetically fix them. An environmental
influence may finally be genetically accommodated if there exists a relevant genetic
variation. What was missing from Lamarckism was that pre-existing physiological and
behavioral adaptability allow the organism to expose itself to environmental changes
and respond successfully.
178 Chapter 4
6. Evolutionarily important novelties in physiological evolution are too numerous to

summarize. They have often been features that impose protective barriers between
organisms and their environment, such as waterproofing in plant and arthropod
cuticles and vertebrate skin and heat insulation in birds and mammals. The invention
of cellulose and lignin skeletons in plants and calcium carbonate shells and calcium
phosphate skeletons in animals potentiated their anatomical evolution. The placenta,
the hypermorphic cerebral hemispheres, and the corpus callosum were immediately
adaptable. It must be borne in mind that key innovations happen in the context of
other generative conditions.
7. Physiological evolution may also be affected by unpredictable contingent factors,

such as the interaction of independent genes to produce new enzymes, or the
interaction of previously independent organ systems. More predictable are
physiogenic contingencies that occur as a result of transition from one environment
to another. Major cataclysms are unpredictable but may have a direct effect on
biochemical functions through heat shock. They also remove competitors and
predators that may have hindered the diversification of organisms with advanced
adaptabilities.
8. Physiological emergences have often produced a constellation of multiple

functions. Glands associated with hair provide for evaporative cooling, milk
production and sexual attraction, as well as maintaining insulative properties of hair.
The most outstanding example is the potential for multiple behaviors that
accompanied emergence of the neocortex.
9. The course of emergent physiological evolution has led to greater self-organization,

independence, and freedom of choice.
10. Most important events in physiological and behavioral evolution occur above the
gene level. Evolution is not a process of changes of the distribution of alleles in gene
pools. It involves instead the reality of the organism, which represents the past and
shapes the evolutionary future.
A Note on Plant Physiology

Some, but not all of the concluding generalities above apply to plant physiological
evolution. I will bring the subject back in chapter 9 under physiological theory. I
have not neglected the plants out of indifference or incompetence, but because I am
constrained to limit the size of the book.
5
Development and Evolution
The major empirical fact about the development of animalsa fact which has no theoretical
inevitability, but which is so obtrusive that only the rudest observation is necessary to establish
itis that the end-products which it brings into existence usually vary discontinuously.
C. H. Waddington, 19571
If evolution is emergent, the basis for this is to be found, not in the natural selection of random
mutations but in the creative potential of epigenesis.
M.-W. Ho and P. Saunders, 19822
. . . an empirical approach to the problem of novelty has to focus on the organizational principles
of developmental systems and their ability to generate new structures.
G. B. Mller and G. P. Wagner, 19913
Before Darwinian theory, it was known that many animals, diverse in their mature
forms, shared anatomical homologues that must have arisen by the same basic
processes of development. Darwin concluded that they must therefore have evolved
from common ancestors. However, efforts to elucidate developmental evolution was
more intense among neo-Lamarckists, who did not object to its saltatory implications.
Furthermore, long before the molecular structure of the gene was worked out it was
realized that the diversity of organisms was not to be understood in terms of different
gene complements but in terms of different expressions of the similar sets of genes
that all organisms possess. Von Uexklls metaphorical piano, with its keyboard of
Mendelian genes, did not have to be reconstructed or given new keys to create
different music, only played according to different instructions in the scores. In the
language of modern biology, the structural genes that code for proteins are similar
across the biological spectrum from bacteria to humans. Even regulatory genes are
highly conserved. Although the number of protein domains that are coded in DNA is
far smaller than the number of genes, they can be arranged and rearranged in different
combinations. What has changed during the course of evolution is the set of instruc-
180 Chapter 5
tions for differential gene expression and protein domain combinations. And these, in
combination with gene duplication and differentiation produced more and more
complexity as time went on. This message has not completely sunk in. Some biologists
still believe that the natural selection of random point mutations that improve
ecological fitness is the essential or ultimate process of evolution. Everything else is
proximate, or contributory, as well as random. For them, complexity is an accidental
accretion of adaptational molecular changes. Molecular biologists were taken aback by
the genome projects discovery in 2001 that a human has only 10,000 more genes
than a simple roundworm. For von Uexkll, however, it would still have made sense
if we had been found to have fewer genes.
Most non-biologistssometime less myopic than the specialistsidentify evolu-
tionary diversity with differences in form, or anatomy. These are caused by alterations
in developmental patterns in conjunction with changes in gene expression and
environment. C. H. Waddington could not bring himself to say that developmental
evolution is saltatory. But in his epigraph he admits that epigenetic divergences are
discontinuous in their phenotypic manifestations, as Geoffroy had proposed before
Darwinian theory came along. Mae-Wan Ho and Peter Saunders help us focus on the
emergent nature of developmental evolution. Gerd Mller and Gnter Wagner infer
that the generation of novel organization is saltatory. Such implications have always
made the gradualistic Modern Synthesis wary of incorporating epigenetics. Another
troubling prospect is that the environment can have a directing effect on the course
of developmental evolution, and that brings in the physiology and behavior of the
whole organism too. If that were not enough, I am going to rub salt in the wounds by
resurrecting orthogenesis in chapter 7. However, I am not addressing the fainthearted
here. They have long since left the field to the travelers who have persevered out of
interest in evolutionary origins and diversity, and dissatisfaction with neo-Darwinist
gradualism.
Now that we are at the developmental ring of the evolutionary circus, with its
liveliest of performances, it is salutary to recall where we have already been. In the
symbiosis and association ring, the raw material for natural epigenetic experimenta-
tionsexually reproducing, eukaryotic cells in multicellular groupingshad already
come into existence. Moreover, evolutionary physiology and consequent behavioral
flexibility of the organism operate in an adjacent arena, and these three rings of the
evolutionary circus are all linked under the big top of the environment. Therefore, we
should not let the razzamatazz in a particular ring mislead us to think that it is the best
of the show, and to forget the others. While the circus metaphor serves to simplify the
causal complexities of evolution, the reality is the whole organism in its environment,
bearing in mind also that the environment consists to some extent of other organisms
of the same and of different types.
Development and Evolution 181
Perceptions of Epigenesis and Evolutionary Development
A quick primer in some of the modern terminology for embryological or developmen-

tal evolution is needed at this point. Epigenesis is archaic, being Aristotles term for
the embryonic ordering of a complex being from disorganized matter. It is now
synonymous with the general process of embryonic development. With regard to the
importance of embryology for evolutionary theory, J. H. Woodger (1929) wrote:
What we do observe . . . is a gradual rise in the level of organization of the developing
organism, i.e., this appears to be beyond reasonable doubt an epigenetic process.4
Epigenetics, as it was used by C. H. Waddington in 1942 and 1957, meant the study
of developmental processes that involved differential gene expression, and its
regulationhow the genotype gave rise to the phenotype. In Epigenetics (1974), Sren
Lvtrup defines it as the study of anything that affects normal or evolutionary
epigenesis, including the role of non-DNA influences, both organismal and environ-
mental. The definition of epigenetics is the subject of some ongoing etymological
debate, which has even run as a Socratic dialogue in the pages of Science.5
Some definitions limit epigenetics to heritable mechanisms, pertaining to DNA and
its regulators. But that is too narrow, since development can be affected consistently
and persistently by non-heritable environmental factors. And some environmental
influences are heritable though no DNA changes are involved. Evolutionary
epigenetics considers how changes in epigenesis might result in anatomical and phys-
iological change. Like Lvtrup (1974), I take epigenetics to encompass all of the
mechanisms of epigenesis, including its evolution. Its scope includes alterations of
gene expression, the effects of the exterior environment, the internal milieu
including the influence of symbionts, the interactions of embryonic cells, the
cytoplasmic environment, and the process of genetic assimilation of environmental
effects. Some modern authors prefer the term evolutionary developmental biology,
which they feel better captures the entirety of embryology in relation to evolution.6
They are the ones who call themselves evo-devos.
Theoretical connections between development and evolution had been established
before the publication of The Origin of Species. The quasi-evolutionary paradigm called
nature philosophy, which proposed a unity of plan among organisms, inferred the
relatedness of organisms based on similarities of anatomy. Out of this school of
thought came Goethes ideas on plant and animal homology, and Owens concept of
the specially created archetypal organism, whose anatomy diversified to produce
different homologous structures. Nature philosophy co-existed with Lamarckian evo-
lutionary theory, and both were integrated with developmental evolution by
Lamarcks colleague tienne Geoffroy de St. Hilaire, usually referred to simply as
Geoffroy.
182 Chapter 5
Geoffroy promoted the importance of understanding epigenetic processes of

evolution. He believed that species diverged from common ancestors through
alterations that the environment induced in their developmental pathways. The
earlier in the developmental process that the alteration took effect, the greater would
be the change in the mature organism. Those insights should have guaranteed a strong
epigenetic component to all subsequent evolutionary thought. But he over-
generalizedas T. H. Huxley remarked, he spoiled his case by stating it. For example,
he proposed that all that was needed for a vertebrate to emerge from a protostome like
a squid was reversal of the dorsoventral axis. Nowadays, the study of deep homology
at the gene level brings us much closer to Geoffroys position, although the reversal of
the dorsoventral axis would have occurred in very early ancestors of the protostome
and deuterostome lines, rather than in a squid or a fish. However, his contemporary
Charles Darwin shied away from any such saltation, because it would reduce the
causal power of natural selection. Embryology only mattered to him for evidence to
support the evolutionary relationships of different animal families.
It should already be evident that much of evolutionary development remains a
tangled bank of speculative suggestions, well-described processes, some molecular
mechanisms, metaphysics, and wishful thinkingincluding a dysfunctional relation-
ship with selectionism. To bring a degree of order to my discourse, I will first take the
route of describing individual developmental (ontogenic) changes that indicate how
evolution might have occurred. Then comes the problem of understanding what kind
of ontogenic plasticity allows change without disintegrity. This, in turn, provides some
answers to the question of how radical phylogenetic or evolutionary changes are
accommodated.
Good Sports
The most familiar examples of epigenetic stability and developmental change are to
be found in plants and animals in our homes, gardens, and farms. Also, when we look
in a mirror in a reflective frame of mind we recognize uniqueness, similarity to close
relatives, and a connection with our distant primate relatives. Individuals who are
abnormal provoke thoughts about how they might have come to be that way. As
Aristotle said, nature is true to typedogs beget dogs and cats beget catsbut there
are odd exceptions that breeders call sports, which are quite distinct from their
parents in some way. The conditions of confinement for breeding animals, as well as
deliberate selection for tameness, may all be epigenetically destabilizing, inducing the
production of developmental novelties, even when the breeding stock is not closely
inbred.7 Good sports are chosen as the founders of new pedigrees. Broadly they remain
true to type, but not to form, as Darwin very well knew. He was fascinated by pigeons
with feathered feet and webbed toes, fantails with multiplied tail feathers, and others
with extra vertebrae and elongated beaks and bones. He did not even stop to think of
them as saltations, although he accepted Sir John Sebrights word that he would
produce any given feather in three years, but it would take him six years to obtain
head and beak.8
One of the most frequently cited sports in the Darwinian era was the Ancon ram,
which had very short legs, and was selected by American breeders because its progeny
were easier to fence in than the normal long-legged form. Note well that in farming,
as in nature, the developmental saltation comes first, followed by the act of selection,
whether conscious, natural, or metaphorical. The dachshund is another familiar short-
legged sport that was selected for its ability to hunt badgers in their setts without
knocking its head against the roof. Both the Ancon ram and the dachshund result
from the premature completion of limb bone ossification, similar to the condition in
human achondroplasic dwarves, who have almost normal trunks, but short arms and
legs. Such phenotypic conditions may be caused by a variety of epigenetic hormonal
changes. Apart from dwarves there are other human growth enormities, such as
pituitary midgets and giants, and pygmies. Although the word enormity suffers
from usage slippage, its proper sense of out of the norm seems to be more
appropriate than abnormality; African pygmies regard the rest of us as abnormal.
Acromegaly is a burst of growth of the extremities near the end of development, which
increases the dimensions of the jaw and hands and feet. It is another common
expression of human developmental hormonal effects, based on alterations in gene
expression, but with some environmental influences such as diet as well.
Geoffroys evolutionary thinking was influenced by his study of abnormal human
embryos and fetuses, for which he coined teratology.9 He mistakenly believed that
the origin of the change was in the developing organism. Or was he in error? By
modernist lights, if it does not occur in the germ plasm of one of the parents it is not
heritable, and therefore meaningless in an evolutionary sense. But Geoffroy also
thought that the environment could directly cause such changes, and keep on causing
them from generation to generation, and I will not exclude this as a contributory evo-
lutionary factor. For Geoffroy, birds might have arisen from reptiles by such an
embryonic saltation. And he did not hesitate to conclude that such was the
mechanism of the origin of species, which is how he phrased it in the title of his
1833 memoir. In Geoffroy there is an element of truth that has to do with the genetic
fixation of phenotypic changes, or genetic assimilation, all of which will be dealt with
shortly.
With Geoffroy came the first musings about processes and mechanisms of develop-
mental evolution. These influenced German embryologists, such as von Baer, who
were to lead the discipline for the best part of a century. In 1864, von Klliker argued
that Darwins gradualism was inadequate to explain progressive evolution. His
alternative was the emergence of novel forms through sudden embryonic metamor-
phoses, like those that gave rise to medusae from polyps and adult echinoderms from
184 Chapter 5
their planktonic swimming larvae. In response to von Klliker, T. H. Huxley repeated

the notorious remark that he had made to Darwin that The Origin of Species was
hampered by unrelenting gradualism and that saltations might be possible.10 The
modernist view is that metamorphosis does not represent evolutionary saltations, but
are compactions of previously gradual developmental processes. This is not contra-
dicted by epigeneticists, but they see that metamorphoses have another evolutionary
significance, since they are life cycle stages where the developing animal might have
a variety of evolutionary epigenetic options.
J. J. Murphy (1869) argued that evolution must be a matter of differentiation and
integration, and phylogeny followed ontogeny. This inspired Darwins critic St.
George Jackson Mivart to propose that saltatory evolution, manifested during
development, would help to solve one of the problems of gradualism: how the
incipient stages of a gradual process could have selective value.11 There was no such
gradual phase, just a creative saltation. His other explanation, an autonomous drive,
will be discussed in chapter 7. Mivart also took neoteny to be a kind of developmen-
tal saltation, albeit a leap backwards. And he puzzled over parallel evolutionary
patterns that appeared to have more to do with inherent developmental trends than
with adaptation.
The American neo-Lamarckist Edward D. Cope made an important theoretical con-
tribution to developmental evolution by emphasizing the importance of changes in
relative developmental timing, such as acceleration and retardation. These could cause
more complex allometric shifts if the relative rates of development in different cell and
organ lines were affected. Acceleration of the growth of the front end of an okapi
would produce the long neck, heavy pectoral girdle and strong front legs of a giraffe,
the development of the rear end being retarded. Relative changes in timing and rate
now come under the heading of heterochrony. Cope also theorized that by his Law
of Repetitive Addition, a simple organism could become complex through multiplica-
tion and then differentiation of its body segments. This concept, which I have
renamed repetitive differentiation, applies just as well at the molecular level, and I
have already discussed its importance in physiological evolution.12
Before he became an emergentist, Conwy Lloyd Morgan appreciated the need for a
generative theory of evolution to complement the Darwinian description of what
happened after change had been generated. His Animal Life and Intelligence (1891)
focused on the importance of variation. In addition to superficial variations that
involved color and external form, there were organic variations of physiology, and
behavior, and reproductive and developmental variations, which included hete-
rochronic alterations in epigenesis. Natural experiments in development might result
in saltatory evolution; but increased organismal complexity was a response to
increased environmental complexity, as Herbert Spencer had proposed. Later he would
shift that stance to become an emergentist committed to discontinuous endogenous
change in complexity, albeit with environmental influences.
William Bateson is now remembered for popularizing Mendelian heredity, and

coining the name genetics. Although he studied at Cambridge under a strictly
Darwinistic, comparative embryologist, F. M. Balfour, he leaned in the direction of
neo-Lamarckism and saltationism. The director of his study of Balanoglossus in the
United States was W. K. Brooks, whose Theory of Correlated Variation prompted Bateson
to explain how complex innovations arose.13 Minor changes in the internal
embryonic environment could trigger correlated changes in associated systems. If
some such accommodatory mechanism did not exist, developmental saltations
would have been too disruptive to ever make a contribution to evolution.14 Bateson
set out exhaustive research results in Materials for the Study of Variation with Especial
Regard to Discontinuity in the Origin of Species in 1894. In it he proposed that there had
to be natural saltatory tendencies of progressive variation, but by that time he had
rejected the notion that the environment had a direct influence on evolution.15 As the
title and publication date of Batesons book suggest, he was already ahead of Hugo De
Vriess Mutation Theory of evolution, which he promoted on its publication just after
the turn of the century.16
Just after T. H. Morgans Drosophila group began to focus the attention of evolution-
ists on genes and chromosomes, Hans Spemann and his contemporaries discovered
that while nuclei affected differentiation, determinants from the cytoplasm of
surrounding cells could have a feedback effect on them.17 Spemann himself did not
give any great weight to the evolutionary significance of the organizer effect, being
more concerned with experimental facts than theoretical speculations.18 Indeed the
history of developmental biology indicates two categories of investigator. The first was
pragmatically interested in a comprehensive factual description of embryogenesis and
the details of its processes and mechanisms. The second was more concerned with
theoretical interpretations in an evolutionary context. A synthesis of epigenetics and
evolution was retarded by the indifference of the pragmatists, and lack of evidence to
support speculation. Moreover, the theorists alienated gradualistic evolutionists by
concluding that developmental evolution had to be saltatory.19
Good sports need to be cosseted by breeders, and guarded from genetic mixing as
well as being selectively bred. Isolation of some kind is assumed to be an essential part
of natural speciation. But, could they take care of themselves in the struggle for
existence in the wild? Gradualists argued that developmental saltations were too dis-
integrative for them to survive at all, far less to contribute to progressive evolution.
The neo-Darwinist R. A. Fisher wrote in 1930 that macromutational leaps of Nature
could only produce damaged goods. Because they had eluded the benign attention of
natural selection, saltatory deviants could not survive. For example, the bithorax
condition in Drosophilaan extra pair of wingscould not be functional, because its
nervous system was not properly coordinated for flight with four wings. This is true of
bithoracic wings in fruit flies, but most other insects have two coordinated pairs of
186 Chapter 5
wings, and primitive flying insects managed to accommodate without detriment the
development of multiple simple wings in many body segments, through some change
in developmental regulation.20 And this was followed by other phenotypic saltations
resulting from the repression of wing development from all segments except a pair in
the thorax.
Echoing Fishers objection to a role for macromutatory saltations in evolution,
Rupert Riedl, in Order in Living Systems (1978), uses the metaphor of a high-rise
building under construction. If the builder misreads the basement plan and puts the
elevator well in the wrong position, and if the plans for the other floors are then read
properly, the elevator will never be able to leave the basement, and the building would
be unfit for habitation. But just as a builder could modify the old plans and finish con-
struction so that the elevators would work, so could an organism accommodate an
early error. For instance, veins in the wings of young insects guide the path of
developing nerves. Yet, in the absence of crucial veins in some mutant insects, the
neurons manage to find new and effective developmental routes, and induce the
appropriate sensory organs when they reach their goal.21 Moreover, many insects
make major morphological changes in their larval basements, such as multiple,
atavistic legs in caterpillars, and yet come back to the original form of the adult.
The regulation of epigenesis in ways that keep the organism true to type involves
back up systems that allow the usual goal to be reached despite potentially debilitat-
ing mutational losses or modifications of gene products. One example in human
development is syndactyly: what starts out as a six-fingered embryonic hand becomes
the usual five-fingered appendage, because two of the fingers fuse into one. Bateson
was right that there are accommodatory mechanisms, and we are coming to
understand them better. So we know that an epigenetic elevator well that has been
misplaced in the basement can accommodate itself by inducing architectural changes
in the upper floors. There are some clearly established ways in which the old plans can
be junked, a divergent design followed, or a new design superimposed, which we will
explore later in this chapter. Some epigeneticists are not aware that there ever was an
accommodation problem, which shows that ignorance of history can occasionally
mean liberation from big issues that were never really significant. The crucial point
is that accommodatory mechanisms not only keep development true to type, but
might compensate for detrimental consequences when a radical epigenetic change
leads off in a new evolutionary direction.
Hopeful Monsters
After Mivart focused on the good sport as a model for epigenetic evolution, the next
development of the idea came in the form of the hopeful monster (Goldschmidt
1940). Its creator had good grounds for seeking alternatives to selection theory, since
his extensive field studies on Lymantria, the gypsy moth, showed that Darwinism
encompassed only minor elements of evolution, affording no clue to progressive

change. Before the hopeful monster was conceived in 1933, for a lecture at the
Chicago Worlds Fair, Goldschmidt had already considered heterochrony in
development, and mused that the accommodation mechanism that would buffer
radical embryonic alterations must be a coordinated shift, like the operation of an
automatic transmission in an automobile. The major criticism leveled at Goldschmidt
nowadays is that he did not try to explain how any kind of monster would be fit
enough to survive, far less come to dominate a population. He did admit that an
experiment like the tailless Manx cat was just a monster. But Archaeopteryx, a
feathered reptile, was a hopeful monster, because it could put its feathers to some use
for gliding, if not true flight. He should have asked himself how just-a-monster could
persist long enough for him to characterize it. The answer is that it retains organismal
integrity, and its monstrosity is neutral or of minor relevance to competition and
predation until perhaps a catch-it-by-the-tail predator comes along. The Goldschmidt
toad reported by David Rollo (1994) as doing very well in an Ontario garden, had
functional eyes that had developed in the buccal cavity from the roof of its mouth.22
No doubt there would be a selective pressure for that oneseeing its way better to its
food perhaps? But it was a saltation nonetheless. Roy Pearson (1999) points out that
among wild starlings there are sports with long bills reminiscent of nectar-feeders. One
was observed to feed normally, without any obvious disadvantage. Whether an
innovation, or an atavism to a nectar-feeding ancestor, the phenomenon is probably
a saltation involving unusual neural crest cell action and morphogenetic protein
production.23
The just-a-monster features of some human terata have afforded not only hope, but
success to some other vertebrates: giantism and achondroplasic dwarfism are natural
in otters. The armless phocomelic condition, where the hands emerge from the
shoulders, brought to public attention by the thalidomide scandal, is not monstrous
in a seal; and complete limblessness is typical of snakes, as well as some lizards and
urodele amphibians. Although some of these examples can be interpreted after the
fact as being adaptational to particular habits and habitats, the initial emergence is by
developmental saltation, and the primary requirement is organismal wholeness,
which is causally prior to the tests of natural selection.
One of the monsters hopes is to have other monsters to mate with, so that its new
qualities will be passed on to the next generation. In organisms that can clone
themselves or self-fertilize there is no such difficulty. Plants and primitive animals that
produce vast numbers of gametes could establish instant populations of the new type.
For the others, the condition that arose in their parents germ cells might emerge in
only a few siblings, and require close inbreeding to establish a distinct new lineage
within the species. Recessive alleles associated with monstrosity in the homozygous
condition could accumulate by genetic drift and so eventually produce a larger
broodstock.
188 Chapter 5
If it is not better at what its parents did, the emergent will be obstructed by
established patterns of competition and predation. If it is physiologically adaptable,
alternative environments or habits proffer great hope. The proto-bird can take to the
air, and the proto-otter to the water. Monsters with greater adaptability than their
parents may still have to wait until a radical change in the existing environment has
occurred, or head for the fringes. So much for the fate of epigenetic novelties once
they have occurred. Questions remain: how do they get over the normal developmen-
tal constraints, and when they do, how is it that their natural epigenetic organization
doesnt fall apart? I will begin to answer this by looking at ontogenic plasticity, or the
scope for deviation that exists in the development of an individual organism. In the
higher plants, extensive phenotypic plasticity helps to offset the occasional disadvan-
tage of having to remain rooted in the same spot for life.24 Animals are much more
predictable in their final mature form, but they have more flexible habits. In both
cases, epigenetic and physiological adaptability provides some room for maneuver.
Epigenetic Plasticity
In the physiological arena we saw two major types of adaptability. The first accommo-
dates to change by switching to mechanisms that keep it going, e.g. when the
temperature changes, the enzyme with the matching temperature optimum is turned
on. The internal milieu may change; but the operational efficiency of the organism is
not affected. Alternatively, external change is buffered by homeostasis and internal
stability is maintained. In development there can also be an accommodatory switch
called facultative phenotypic expression, an either-or choice described by Mary Jane
West-Eberhard, where condition-sensitive expression of alternative phenotypes
means that in a variable environment a novel phenotype (such as worker behavior, or
a new trophic specialization) can evolve alongside an established specialization
without being expressed (competing) in the same situations.25 This describes circum-
stances where the same genotype can give rise to two distinctly different phenotypes,
the switch being activated by an environmental cue. In termites, and presumably
other social insects, the timing of the supply of food and the effects of juvenile
hormone modulate the caste system. The relative numbers of workers and soldiers are
adjusted according to the needs of the nest.26 Boris Uvarov detailed striking examples
of novel phenotypes that appear in response to population density in his encyclope-
dic work, Grasshoppers and Locusts (1966, 1977). At low population levels the adults are
drably colored and solitary in their behavior. With increasing population the egg-
laying behavior of females changes so that they lay eggs en masse, so that the deme
density is increased, and the adults of several species become vividly colored and
striped. The crowded wingless hopper stages of locusts form marching bands.
Eventually as adults they may take to the air in flying swarms that can cover an area
as large as 780 square kilometers. Such behaviors are stimulated by acoustic and visual
cues, and modulated by juvenile and sexual hormones. These kinds of plasticity
involve an all-or-none commitment for the individual, and lacks the modifiability
associated with physiological and behavioral adaptability. Nevertheless, it illustrates
that mechanisms that keep development predictably on track can, under some cir-
cumstances, be derailed without lethal disintegrity.
Whether an accommodated change makes any difference in selective value or not,
the new epigenetic experimental organism will be ready to go about its life in a novel
way if its integrity is preserved. The semi-independence of developmental pathways
has to be sufficient that change in one does not act to the detriment of others. Yet
there has to be enough feedback between the pathways to make integrating
adjustments. West-Eberhard (1989) notes that epigenetic shifts are further accommo-
dated by the plasticity of behavior and correlated functional anatomical shifts. She
gives the example of Slijpers goat, which was born with very short front legs and
normal hind legs.27 But this good little sport learned to walk upright, and its
anatomical development responded with accommodatory changes in the spine,
thorax, neck and muscle insertions. There is no argument that the epigenesis of an
individual is plastic, which being so, the difficulty of adjustment to change is
mitigated and monsters might not be altogether hopeless. Historically, however,
accommodation presented a major theoretical problem.
The Canalization Bind: Does Lack of Plasticity Obstruct Evolvability?

Aristotles aphorism that nature is true to type is so consistent that it presents evolu-
tionists with the perennial dilemma of understanding how it works, and how it might
be overridden. Although he knew of the existence of abnormalities in human
development that survived to maturity, he argued that the soul had a quality called
entelechy that ensured that cats begat cats. The dilemma was emphasized for
materialist Ivan Schmalhausen, because he could see that developmental stabilization
became more rigid with the passage of time, as external environmental triggers
became internalized in the organism. But he had a good general idea of how to resolve
the problem. Entelechy was then re-invented by Waddington (1957) as
homeorhesis, which signifies the stabilized flow of epigenesis. The thing that is
being held constant is not a single parameter but is a time-extended course of change,
that is to say, a trajectory.28 Thus, the organisms development is kept on track by
compensations for minor misguiding influences.
Waddington distinguished the processes of homeorhesis and physiological
homeostasis. He did not, however, completely round the circle by comparing their
evolutionary roles. Homeostasis allows the mature organism to persist in its being
while exploring new environments, and acquiring habits that might otherwise tend to
disequilibrate its internal milieu. It places no obstacle in the way of functional
anatomical change that would complement new behaviors in new environments,
190 Chapter 5
quite the opposite. Homeorhesis does, however, obstruct anatomical change by

conserving the integrity of the original form. Therefore homeorhesis cannot be
equated with evolutionary adaptability in the same way as physiological homeostasis.
Nevertheless, anatomical changes have occurred, and, as Peter Saunders points out,
Homeorhesis is a necessary property of an epigenetic system. But a system which
possesses this property will also have the capacity for heterorhesis, i.e., for large,
organized change.29
Developmental adaptability is inversely correlated with Waddingtons canaliza-
tion, the degree of fixation of epigenesis along particular developmental pathways.
The concept of canalization arose from the well-known metaphor of the epigenetic
landscape. Imagine a water-eroded slope, where minor channels would run into large
channels as they flowed downhill. If a round stone is randomly pushed from the ridge
at the top of the slope it will eventually find its way into a minor channel, whence it
is canalized by a deeper channel in a determined downward direction. At first, the
kinetic energy of the stone, and the shallowness of the channel, might make it bounce
away from its likely course. This would be loose canalization. Eventually, however, the
stone would roll into one of the lower, and deeper channels, from which its escape
would be difficult, and its final goal all but certain. The behavior of the rolling stone
offers an heuristic metaphor for the migration of embryonic organizer cells as well.
Both of them slow down, are obstructed, and eventually gather moss which fixes
their position firmly. Tight canalization prompted the crucial question of how it could
be loosened sufficiently for epigenetic evolution to occur. Waddingtons model
suggested disequilibria in the topography of the landscape itself, and his equation
included disruptive alterations in the real external environment.
It is often argued that the body plans of animals that emerged around the time of
the Cambrian explosion have become so tightly canalized over geological time that
further evolution is impossible. But the vertebrates are exceptions that prove the rule.
They modified the basic plan, made novel additions, and kept on doing it. In hominid
evolution the process has been rapid by conventional calculations. These changes are
epigenetic, and therefore decanalization and accommodation can be quite radical,
despite the passage of time and the growing defenses of homeorhesis. The question
remains: what are the circumstances that bring such changes about? Or how, as
Waddington asked, does nature get away with it? Schmalhausen had already suggested
that physiological adaptability in the developing embryo, and in the mature hopeful
monster, provided some accommodation.
Even stable environments can cause phenotypic changes, especially where there are
distinct climatic and photoperiodic cycles. There is also room for adaptational special-
ization in microenvironments within stable environments. Finally an ecosystem will
contain a diversity of specialists. The more specialized an organism becomes in a stable
environment, the more it is locked into a line of evolution that can only go in one
directionmore of the same, whether by directional selection or allometry.

Exploration of alternatives is increasingly prohibited by competition; and with
specialization there comes a more rigid epigenesis, loss of plasticity, and a diminishing
ability to find new options.
The Specialization Bind

Long before Waddingtons attempt to formalize the problems of evolutionary
development, zoologists were aware of incongruities in the line of animal evolution
leading to the vertebrates. Sedentary echinoderms and sessile sea squirts, which have
stayed the same for 500 million years, seem to be in the specialization bind at which
Cuvier originally hinted, with form and function so well integrated and adapted to
their conditions of life as to be impossible to alter. How could vertebrates have arisen
from such creatures? The answer lies in their larvae, which have potentially greater
behavioral and morphological plasticity than the specialized, sedentary adults. If they
fail to metamorphose to the inflexible adult form, but still become reproductively
mature, they have more scope for alternative behavioral and morphological changes.
It might be argued that these particular specialization locks are altogether spurious, if
the larvae represent the mature morphology of common ancestors, and echinoderms
and seasquirts side-branches that quickly reached dead-ends. But the larvacean uro-
chordates, which are tadpole-like swimmers, unlike their sessile seasquirt relatives,
clearly illustrate the possibility of drawing back to juvenile plasticity. And their
ancient relatives could then have leapt in new directions. Paedomorphic repression of
multiple limbs was a particularly important step in the line of evolution that led to the
insects, although the typical adult form that was finally established is curiously
inflexible.
Radical evolutionary change in body pattern through paedomorphosis was a
distinct possibility that met no serious objections from any quarter. Nor was there any
opposition to the idea that there could be add-onsevolutionary changes later in life
that would not interfere with normal development. The question of how novel body
plans could evolve from the plastic larval forms was open. Geoffroy and later saltation-
ists had suggested that the earlier an alteration in development occurred, the more
radical would be the ultimate change in body form. However, this option was strongly
resisted, for the reasons that Fisher gave, and because it threatened neo-Darwinist
gradualism: saltations would undermine the necessity for natural selection to have
acted persistently on a graded series of slight changes in order to produce its evolu-
tionary effect. The hypothetical mechanism could only be saved by rejecting the
possibility of saltations.
In The Ghost in the Machine (1967), Arthur Koestler referred to evasion of the special-
ization bind as reculer pour mieux sauter. If the embryo first stepped back it might
make a better leap to evolutionary novelty. The concept was known almost a century
192 Chapter 5
earlier when it was brought to the fore by Walter Garstang. A well-known example is
that of the axolotl, a neotenous tiger salamander, whose sexually mature tadpole does
not metamorphose because of an epigenetic change involving prolactin and
thyroxine. Among salamanders there is a full spectrum of these kinds of neotenic
changes. The least canalized may be reversed by temperature change; the intermedi-
ate condition, in the axolotl, can be altered with thyroxine treatment, and the fully
committed condition cannot be experimentally altered. Considering the earlier
diversity of large, heavily armored terrestrial extinct Amphibia, this return to
childhood could be a character of many extant representatives of the class. Drawing
from many animal phyla, Ryuichi Matsuda (1987) gives examples of paedomorphic
simplification of the life cycle and adult morphology, focusing on the effects of the
environment, especially where they affect egg size, and cause rapid reorganizations of
metamorphoses. This is getting ahead of the story, but it might help you to persevere
if you know that the historical speculations are justified by subsequent data.
Time for a brief synopsis of evolutionary life cycle changes that help to loosen canal-
ization and evade or transcend homeorhesis. For the full credit course, start with
Gavin De Beers Embryos and Ancestors (1940), advance to Stephen Jay Goulds
Ontogeny and Phylogeny (1977), and then consult some of the later works on hete-
rochrony, i.e., the process of changing body forms by alterations in the timing and
rates of developmental processesideas set in motion by E. D. Cope. Here I draw
largely on Goulds treatment, which is straightforward and familiar to modern
students. Adding-on to the old adult form is called peramorphosis, and the
extension or exaggeration of particular adult characteristics hypermorphosis. For
orthogenetic hypermorphosis that might hypothetically lead to functional-morpho-
logical instability and possible extinction I use ultramorphosis. Paedomorphosis is
persistence of a juvenile form in the adult. Neoteny is the variant of paedomorphosis
where the animal grows to sexual maturity and adult size at the normal rate, but
retains the juvenile form instead of undergoing gradual or metamorphic change to the
old adult form. This applies in Matsudas examples of talitrid amphipods and
salamanders. The other kind of simplification in form is progenesis, usually
heritable, in which the simple early juvenile form becomes sexually mature preco-
ciously, remains very small, and fails to complete development of the former adult
anatomy. This is common in phyla such as arthropods and mollusks, and, as Gould
deduces, such uncoupling of growth and development is a significant evolutionary
phenomenon. Since the time taken to reach maturity is reduced, several generations
can fit into the time formerly taken for one, although success in this epigenetic arena
is congruent with the larger environment.
The life history of an organism can be altered by cenogenesis, in which a novel
phase is inserted in early development to produce a larva that might be quite different
in its anatomy and behavior from the mature organism. The best known examples are
in insects whose larvae are maggots or caterpillars, which obtain most of the energy
needed for growth, development, and gametogenesis. Finally, the life history meta-
morphoses back to the insect norm, and the biological functions of the imago, or
adult, may be largely limited to reproduction.
The most drastic change in life history is deviation, which occurs early and alters
the functional morphology, and ultimately the behavior of the adult. This is no
evasion of hemeorhesis, but a frontal assault. Ultimately, deviation becomes
genetically fixed and characteristic of the type. But the ontogenic plasticity that I have
just described suggests how deviation is accommodated when it first appears. This
kind of evolutionary novelty is anathema to neo-Darwinists because it negates the
explanatory power of natural selection. But if it can be demonstrated that radical
deviations can be spontaneously accommodated by subsequent embryonic
development, without genetic change, their argument is jejune.
Gavin De Beer subsumed radical embryonic change under neo-Darwinism, but
marine biologist Alister Hardy saw it differently. His father-in-law, Walter Garstang,
had already proposed that ontogenic change in marine animal larvae was a means of
reintroducing evolutionary plasticity, especially in the deuterostome/echinoderm/
chordate lineage.30 Hardy went further, to associate such evolution with behavioral
change and genetic assimilation, in his book The Living Stream (1965).31
Hardy also thought that radical deviations were part of evolution, and in this
context he resuscitated the classical evolutionary problem of vertebrate limb
placement. E. S. Goodrich, who had originally explored the matter in 1913, called the
shifts transpositions. They arise from axially arranged segments or somites, several
of which contribute to a particular limb. But they do not derive from the same somite
sets in different animals. The problem how limb development could be transposed can
now be reduced in part to the triggering action of homeotic genes. These are the
foundation of a homology that goes much deeper than the form and placement of
limbs in a particular class of vertebrates. Over time, the genes themselves have
duplicated and varied, and where they are expressed, limbs appear. Like the variants
of all genes, they exist in every cell in the body, but are repressed where particular
organs are not wanted. Limbs can potentially arise almost anywhere at the appropriate
phase of development. They are placed where they function most efficiently in
relation to the other body structures and behavior. But that does not explain the cause
of transpositionhow could an epigenetic algorithm know where and when to shift
the legs?
The orthodox explanation is that trial-and-error transpositions were sorted by
natural selection. More heterodox is the idea that an epigenetically harmonious
novelty emerges from the egg and goes about some new business in a fit manner. The
best hypothesis lies somewhere between the two. These kinds of accommodations
could be originally have resulted from epigenetic experiments made with limb
194 Chapter 5
structure and placement, without the necessity for improbable co-incidental

correlated mutations in developmental genes. From his study of the evolution of ears,
Keith Thomson (1966) concludes that it required correlated progression, which re-
invents Brookss and Batesons version of Darwins correlated variation. Later data
from molecular epigenetics have not qualitatively improved the idea. In contrast, neo-
Darwinism proposes that key innovations, if adaptive, change the selection pressures
so that a cluster of supporting variations are finally accumulated.
Variant repeats of homeotic genes that stimulate the development of antennae,
mouth appendages and legs in Drosophila are expressed chronologically from anterior
to posterior.32 A similar head to tail progression occurs in mammals. Therefore, as a
general principle, natural experimental changes in the anterior limbs might result in
compensatory changes in the posterior limbs, both in placement and size. It can be
done to fruit flies in the laboratory; why not naturally? Anterior reduction of the
forelimbs might result in a transposition or size increase in the posterior limbs.
Behavioral plasticity is one of the key accommodations of such changes. A monster
analogous to Slijpers goat, with large hind legs transposed too far back, might
attempt a similar balancing act of bipedalism, using the forelimbs as stabilizers or
claspers. Such creatures would find their feet more easily if spared the competition and
predation of natural selection. We only have to go to Australia to find such good
sportskangaroos!
Limbs might go altogether. A proto-snake, for example, with increased segmenta-
tion, and small limbs too far apart to hold up the elongated body, could locomote
without much need for limbs, through emphasizing the archaic sinuous movement
still seen in lizards, and which derived originally from lobefin ancestors. Ontogenic
responses such as scale or rib modifications could have then been genetically
assimilated.
Accommodation of Change in Epigenesis

I have already raised the problem of how radical epigenetic change can be accommo-
dated, and have just emphasized behavioral plasticity with regard to limb
transposition. Earlier I mentioned the accommodation of epigenetic change in
individual development, and dropped a few broad hints about how similar processes
occurred during evolution. Comparative embryology has always suggested relation-
ships between ontogeny and phylogeny. And this has been reinforced by current
developments in the study of genes involved in epigenetic regulation. We need a more
complete picture of how such large embryological changes occurred, how they were
accommodated, and how the resulting hopeful monsters realized their aspirations.
Schmalhausens synthesis of Darwinist and epigenetic thought had no difficulty
with accommodation. He asserted that new differentiations were effected as the
organism responded to different environments. What follows is an almost-verbatim
passage from Factors of Evolution which I have slightly edited (and hence italicized) to
bring out the distinction between adaptation and adaptability, both epigenetic and
physiological:
These became integrated into a harmoniously constructed and functioning entity through regulative devel-
opmental systems and physiological adaptability. A highly plastic organization was produced, so that
both advantageous hereditary variations and functional adaptability harmoniously transformed the
entire organization. In the course of individual development, adaptabilities were supplemented by suitable
co-adaptation of organ functions through stabilizing selection. In this way, the organism always evolved
as a integrated whole and novelties did not destroy the harmony of organization. Indeed, new functional
differentiations increased the heritable complexity of organization.33
That Schmalhausen adduced the latter, in addition to the effects of the environment,
as parts of the whole evolutionary picture is typical of his holistic view of the natural
world. The synthesis is however incomplete, since it does not specify the morpholog-
ical plasticity of plants, and the behavioral plasticity of animals.
Arguments to the effect that radical embryonic change will always be deleterious,
raised by Ronald Fisher, Ernst Mayr (1977), and other populationists, were advanced
to justify the gradualistic worldview, rather than to assess epigenetic evolution.
Without question, the mutation of a structural gene responsible for an epigenetic
hormone or enzyme is likely to be harmful, unless, as is often the case, there is a com-
pensatory suite of back up genes already in situ. Yet, classical examples of
accommodatory development were familiar to C. H. Waddington when he published
The Strategy of the Genes in 1957. For instance, embryonic implants such as eye
primordia not only induced an appropriate array of muscles and nerves, they also
affected the developing brain of the animal relative to the size of the implant. He
called this coordination and integration ontogenic buffering.
Although Waddington did not discuss the specifics of loose canalization and accom-
modatory mechanisms, he realized that the subsidiary developmental pathways,
which he called creodes, have some independence of homeorhesis. Some are quite
plastic, for example the one that deals with the development of the endoderm, the
fundamental tissue layer that forms the gut. Because it has some body space in which
to maneuver, its morphospace is similarly larger, and almost any type of gut can
become epigenetically modified and specialized without affecting the overall
development of the organism. Other creodes of organogenesis acquired some capacity
for differential development long after overall body plans had been laid down. The
evolutionary explorations of migratory neural crest cells in the vertebrates that
affected cranial, ear, eye, jaw, and limb structure continued to have a strong impact in
hominid evolution. These give us further clues to evolutionary plasticity and accom-
modation in development.
Nevertheless, there is still a large gap between what we think biologically possible
and what has actually been demonstrated. Also the fact remains that we do not
196 Chapter 5
repeatedly see natural experiments that result in hopeful monsters raising their lovely
heads in every generation. I have dug tons of clams and looked at thousands of their
juveniles through a microscope without seeing a single deviant specimen, except for
those that have been ontogenically distorted by an unusual substrate. But I was
looking at a type that has probably been generatively entrenched for 200 million
years. If I were a botanist my subjective view would be different. Some of my house
and garden plants show some very distinct changes in leaf and flower color through
somatic mutation. My pink-flowering cactus has just developed flame-colored blooms
from a new shoot. Moreover, if, at any time, you want to see the product of a series of
epigenetic changes that periodically occurred over the last 5 million years, take a look
in a mirror.
Whatever molecular and morphogenetic accommodating mechanisms there might
be, it is obvious that the later in development an epigenetic novelty occurs, the more
likely it is to fit harmoniously into the organismic whole. In fact, peramorphoses,
involving hypermorphosis of established patterns of growth and maturation, and
novel additions to them, are the easiest kinds of natural developmental experiments
to accommodate. Going back to Riedls architectural metaphor; if the original plans for
the high rise have been realized, more floors might be added to a different design, with
hanging gardens, penthouses, satellite dishes, and helicopter pads tacked on as after-
thoughts. These peramorphoses and hypermorphoses might have the potential to
change the fundamental function of the building. The late development of feathers
and hairs from the outermost surface of birds and mammals depends initially on
simple hypermorphic evaginations and invaginations of the epidermis. But the phys-
iological and behavioral consequences of feathers and hairs made them essential
components of bird and mammal emergence.
Ontogenic buffering is now almost axiomatic for evo-devos. For example, Raff and
Kaufman (1983) say that plasticity of epigenesis and adaptability of regulatory
mechanisms are always flexible enough to accommodate epigenetic diversification
once it is initiated. Epigeneticists such as Matsuda, and Balon, also have less trouble
with the accommodation of deviation than Riedl. For them, metamorphoses or devel-
opmental thresholds are nexuses of plastic rearrangement, offering various changes of
direction along new pathways. Gerd Mller (1991), although he nods to the ultimate
causes of neo-Darwinist theory, argues that emergent novelties
arise at the transgression of threshold points immanent to developmental systems, where

sequences of developmental interaction are disrupted or new interactions become established,
and the resulting structure will depend on the reaction norms of the system at that point. This
may directly translate into the adult phenotype or may initially produce a transitory structure on
ontogeny not immediately expressed in the adult. Such transitory structures can later become
expressed in the adult stage of descendants through processes of heterochrony or they can
become future modified and provide a developmental basis for other morphological innovations.
Particular opportunities for the modification of developmental patterns exist during the
transition phases of changing mechanisms in the stepwise formation of organs. Generally it can
be expected that new structures arising are easily integrated into the organism through epigenetic
adjustments of the associated systems.34 [Epigenetic thresholds are points of discontinuity (meta-
morphosis being an extreme example), where the emergences of developing structures are
triggered by a variety of stimuli, some endogenous, some environmental. RR] Novelty can thus
arise as a side effect of evolutionary changes of size and proportion, with the specific result
depending on the reaction of the affected systems. In this scenario the emerging structure becomes
only secondarily a target of selection which will determine its maintenance and persistence throughout
the population; the disruption of a morphogenetic sequence lies at its origin.35 [emphasis added]
Mller illustrates these generalizations with three categories of morphogenetic

threshold change.
The first of Mllers categories arises from modification of body size. In the early
stage of vertebrate skeletal development the total number of prechondrogenic, or pre-
cartilage-forming cells, and the overall size of the limb buds, affect the formation of
the adult limb. The trigger for condensing the centers of cartilage formation may be
as simple as a carbon dioxide/oxygen gradient.36 The number of these cells has been
experimentally manipulated to show these effects. And in nature large animals are
more likely to form extra digits than small animals of the same type.
The second is the epigenetic effect of the relative position of organizer cells, or organ
primordia in the embryo, a factor known since Spemanns classical experiments,
which imitated what in nature had been going on for 500 million years. That the site
of action of morphological change is affected by earlier differential development is
simply illustrated by the development of cheek pouches in rodents. These are either
internally derived, lined with buccal epithelium, or externally derived, and lined with
fur. A very minute position change in the point of pouch invagination makes the all-
or-none difference between the two types.37 This kind of late-development
hypermorphosis is common and non-disruptive. But A. C. Burke (1989) argues that a
similarly small modification of epithelial-mesenchymal interactions in early
development resulted in the saltatory emergence of the turtle carapace, a radical
anatomical structure that appeared suddenly in the fossil record.38 Simultaneous
accommodation of the limb girdles within the rib cage is necessary for the new
arrangement.
Incipient intermediate forms necessary to satisfy the theoretical demands of selec-
tionism may never actually have occurred, and are redundant for a theory of
developmental emergence. I have already mentioned changes in cranial, facial and
tooth anatomy involving neural crest cell migrations that could be saltatory in their
initial phenotypic expression and also show continuing orthogenetic trends. Brian
Hall (1998) reviews historical and current advances in this area of study. An organizer
role for the neural crest has been demonstrated in the evolution of part of the
198 Chapter 5
autonomic nervous system, inner ear structure, and a variety of endocrine glands, as
well as the better-known instances of cranial and facial anatomy. John Fondon and
Harold Garner (2004) have established that at the gene level craniofacial changes
involve various tandem repetitions of codons in cis-regulatory genes. The causal
connection between such molecular changes and the activities of neural crest cells has
not been established. One of the best examples of early deviation that was successfully
accommodated by subsequent epigenesis was discovered by Rudolf Raff and his
associates.39 Early heterochronic changes in the segregation of cell lineages in sea
urchin blastomeres cause novel larval forms in which some primitive features are not
manifested, and others appear precociously. These and other derived features of
direct developers such as changes in cleavage pattern and mitotic rates are dependent
on the heterochronic changes in developmental mode and not on adaptations in the
traditional sense.40
Mllers third category of causes of novel developmental emergences is biomechan-
ical. As early as 1874, the German embryologist His had proposed that folds in early
embryos were caused by the mechanical pressure of differential growth. Gravity phys-
iogenesis certainly had an important impact on proto-tetrapods emerging from water
onto the land. And patterns of cartilage and bone formation are strongly affected by
mechanical stimulation. Tension, pressure, shear and locomotion can all bring about
developmental change. In bird embryos, which begin active movement within the
egg, biomechanical stimuli have a major impact on wing development and are
essential to the shinbones.41 Hydrostatic pressure forces the expansion of some
developing eyes and brains.42 Other triggers of threshold phenomena include
hormones, morphogens, and adhesion molecules, as well as egg size and the kinds of
environmental effects proposed by Ryuichi Matsuda (1982, 1987).
Mller also details how transitory intermediate structures, or interphenes, can be
introduced into development. In the nineteenth century, Haeckel divided these into
palingenetic recapitulatory structures and cenogenetic embryonic novelties. As an
example of the former Mller cites the extra joint in the upper jaw of bolyeriid snakes.
Paedomorphic suppression prevents the fusion of two ossification centers that in
earlier vertebrate evolution rose from two separate bones. In the snake this throwback
morphogenesis provides a double-jointed maxilla allows easier ingestion of large prey.
Cenogenetic novelties are represented by the fibular crest in the hind limbs of
theropod dinosaurs and their putative descendants the birds. This structure appeared
de novo through the growth of a stress-induced cartilage sesamoid. The wishbone (or
furcula) in birds may also have arisen from a transitory stress-induced dermal cartilagi-
nous structure. The same is true of the of pandas thumbs, extra sesamoid digits that
Stephen Jay Gould (1980a) made familiar to a wide audience. Such functional skeletal
elements had to be integrated with the neuromuscular system, and this process was
also mediated in part by biomechanical factors involved in how the animals put them
to use. Sren Lvtrup argued in 1974 that the notochord was a similar saltatory
innovation, and that in combination with the absence of mucopolysaccharide from
the body cavities, the notochord had a major impact on the evolvability of the
chordates. Mller proposes that heterochronic modification of interphenes is
responsible for some epigenetic evolutionary discontinuities. Where they crop up they
could be amplified, and development of the old adult phenotypic characters could be
repressed or lost.
The kind of switching involved in reculer pour mieux sauter effects is also addressed
by Mller. Each point during development where there is a switch in the epigenetic
mechanism, affords an opportunity to change emphasis or qualitatively alter
direction. The vertebrate skeleton, while conservative in its fundamental morpho-
genetic patterninga feature that made vertebrate homologies so evident to
nineteenth century zoologistshas a wide variety of mature forms. Despite the con-
servatism of the system the diversification of these forms must have occurred at early
morphogenetic thresholds, such as between cartilage formation and bone formation.43
Furthermore, radical morphogenetic changes need not involve molecular epigenetic
novelties, but simply the redistribution of their sites of expression, sometimes through
topological rearrangements of cells with crucial inductive functions. David Wake and
G. Roth (1989) call this repatterningyour advancement may depend on how good
your re-connections are.
I will incorporate Mllers other theoretical contributions to developmental
evolution into Re-inventing Emergence and A Theory of Emergence (chapters 8
and 10). Still, it is appropriate here to recall the accommodation question, since he,
along with Stuart Newman, has proposed that major evolutionary processes that gave
rise to animal body plans were largely mechanical responses to environmental
epigenetic stimuli. Genes had only a small part to play, and their significant role in
developmental regulation came after the body plans had emerged.44 This implies that
accommodation was unnecessary at that stage. Any experiment could be tried, and its
survival depended only on simple bodily integrity, including an ability to feed.
Another way of tackling the accommodation phenomenon is by computer
modeling. In Making Sense of Life (2002), Evelyn Fox Keller has focused on the theories
of Garrett Odell and his colleagues, who work with robust epigenetic networks in
insects. Although the initiating mechanisms of segment development vary among the
insects, the segment polarity gene networks are highly conserved. This suggests how
there is consistent segment homology among the insects. Initial models that
attempted to get all the physicochemical and simple biological parameters right did
not match the natural epigenetic processes. They concluded that the robustness of a
system that could accommodate parameter changes derived from the entire system:
. . . not only does the network topology embody many different solutions, but most
solutions are highly robust to variation in individual parameter values. Their next
200 Chapter 5
words are very much in tune with an emergentist view of epigenesis: The simplest
model that works at all emerged complete with unexpected robustness to variation in
parameters and initial conditions.45 The whole is greater than the sum of its parts. But
although these investigations say a lot about how nature is true to type, we still have
to get to the next stage of modeling a system that circumscribes how insects
underwent divergent evolution despite their conserved and robust genetic segment
polarity networks. We know part of the solution to this particular problem: leave the
robust system in place and work around it. Let particular segments go on producing
eyes, antennae, wings, legs, and reproductive appendages. The end products can
themselves be enlarged or elongated or regressed without upsetting the epigenetic
applecart. The lifecycle can be modified allometrically, heterochronically, physiologi-
cally and behaviorally. And segmental conservatism remains strong enough for the
least experienced eye to see that its still some kind of insect.
Not all phyla or orders share the robust conservatism of insects. Whether the
mollusks escaped from segmental regimentation, or never had it at all, they are to be
characterized by evolutionary plasticity instead of morphological conservatism. If the
somites of vertebrates can be compared to insect segments they have undergone much
greater evolutionary changes.
A last word on accommodation comes from Marc Kirschner and John Gerharts 2005
book The Plausibility of Life: Resolving Darwins Dilemma. Assuming cellular molecular
processes are adaptable enough to adjust to genomic mutations, subsequent epigenetic
events provide further modification through exploratory behavior at the cellular
level. For example, alterations in regulatory genes that result in potential anatomical
changes in a pair of limbs can be responded to by the exploratory processes of nerve,
muscle, and tendon development. Regardless of the nature of the genomic change, if
not fatal, subsequent adjustments can be made at all developmental levels. There is no
developmental accommodation problem if there is adaptability to changes at the
molecular level. As can be deduced from the earlier portion of this synopsis that deals
with Mllers practical and theoretical observations, Kirschner and Gerharts treatment
of the accommodation problem does not have chronological priority, but it is the
most accessible of current publications.
If we step back to get a broader view, we might try comparing homeorhesis and
epigenetic evolution with homeostasis and physiological evolution, and discover one
common occurrence. They have both undergone some disequilibration that jolted
them free of their stability, enough for change to occur: not so much that the results
are dysfunctional, but not so little that they return the experimental organism to its
original state. That is why it is so important to study emergences that surmounted the
barriers. The fixation or tightening of dynamic stabilities by the natural selection of
slight adaptational adjustments (or internal selection) within the systems leads to evo-
lutionary inflexibility. Subsystems that are epigenetically adaptable may be culled in
favor of those specialized to respond to the most common stimulus in only one way.
Life that carries on under the scrutiny of natural selection is very different from life
that has been freed from it to emerge as new forms into fresh woods and pastures new.
Direct Environmental Effects and Genetic Assimilation

Earlier structuralistic treatments of developmental evolution were biased in favor of
autonomous changes in functional morphology that would occur regardless of envi-
ronmental conditions. Epigenetic self-amplification, or orthogenesis, is an important
example of such endogenous evolution. However, any organism lives in an
environment that affects its life and influences the future of its descendents. In my
previous chapter on evolutionary physiology I noted how homeostasis in animals was
periodically reset by environmental change and physiogenesis. Schmalhausen and
Waddington realized that these factors were important for developmental physiology
as well, and that this provides a key to the escape of the insects and the vertebrates
from the homeorhetic lockup. Did the sameness of the old marine environment
contribute to the evolutionary stagnation of its denizens, while the differences of the
terrestrial environment opened the experimental laboratory for new emergences?
Neo-Darwinism insists that new environments provide different strong selection
pressures that simply elicit appropriate innovations. But I have gone to some trouble
to show how the interplay between physiology and behavior can produce internal
physicochemical changes, prior to any genetic assimilation and subsequent adapta-
tional adjustment.
Just how important are the direct effects of the external environment, and the
internal milieu in developmental or epigenetic evolution? Ryuichi Matsuda catalogues
seventeen phyla in which there are cases of metamorphosis being subject to environ-
mental influences in Animal Evolution in Changing Environments with Special Reference to
Abnormal Metamorphosis (1987). The biochemical epigenetic processes of salamanders
provide the best established illustrations of environmental effects and genetic assimi-
lation. But arthropods offer almost as complete an inventory of known pathways.
Further examples of major phenotypic changes induced by the environment in
animals that undergo metamorphosis are offered by Scott Gilbert and his associates in
Metamorphosis: Postembryonic Reprogramming of Gene Expression in Amphibian and Insect
Cells (1996). In chapter 3, I pointed to epigenetic changes brought about by micro-
organisms such as those that induce the broad thallus of the sea-lettuce;
nitrogen-fixing bacteria that stimulate root nodule growth in terrestrial plants; and
gut commensals that influence the postnatal development of mouse guts, as well as
firing up the immune and digestive systems. I also speculated that symbionts could
have epigenetically effected allometric shifts in giant tridacnid clams, and bivalves
with sulfur-oxidizing symbiosis. A localized internal increase in nutrients could have
initiated these processes. Some of these associations may have been in existence for
202 Chapter 5
hundreds of millions of years, consistently affecting development without being

determined by the genes of the developing organism. It is possible that some gene-
swapping has occurred, as it did between endosymbiotic organelles and their hosts.
What of it? The environment induces changes. Nobody is going to argue, unless it
is also proposed that these changes can somehow become heritable. Recollect that in
his discussion of homeodynamics Roy Pearson notes that the endocrine system that
affects epigenesis in vertebrates is already present and heritable, requiring environ-
mental retuning to have an evolutionary impact (q.v. coda of chapter 4). But several
modern epigeneticists propose a more radical neo-Lamarckist approach. How then
could environmentally induced changes in the organism become genetically fixed,
beyond gene acquisition from symbionts and retroviruses? It does not require the
inheritance of acquired characteristics, but modification of genes, and of a variety of
organismal resources that already exist. The subject has been treated most thoroughly
by Eva Jablonka and Marion Lamb in Epigenetic Inheritance and Evolution (1995). To
date, Mary Jane West-Eberhard (2003) offers the broadest exploration of the general
topic of environmentally-induced change and organismal response.
One of the processes triggered by environmental induction was called genetic
assimilation by Waddington, but the central idea was first published independently
by three different authors, C. L. Morgan, J. Baldwin, and H. F. Osborn, in 1896. The
different shades of meaning and intentions of the originators, as well as those of
Waddington and Matsuda are tabulated by Brian Hall (2001). His citation of the King
and Stansfield (1984) definition of genetic assimilation is worth repeating here:
[Genetic assimilation is] the process by which a phenotypic character initially produced only in
response to some environmental influence becomes, through a process of selection, taken over
by the genotype, so that it is formed even in the absence of the environmental influence that at
first had been necessary.46
The originators of the concept were all intrigued by how phenotypic changes, induced
by environmental changes, through behavioral changes, became heritable. For
example, calluses are caused by skin abrasion in land vertebrates, yet in ostriches, and
in some humans, calluses appear without any preliminary abrasion. Birds that inherit
their songs seem to have followed a lineage that originally had to learn them from
their parents. How did this genetic fixation take place? Darwinists rationalized such
environmentally induced changes as manifestations of a pre-existent genetic
propensity that was then enhanced by selection. The callus is a protective structure,
so any mutation in the direction of callusing would be advantageous. But calluses do
not appear randomly all over the body, to be sorted out by selection according to life-
style needs. It is environmental abrasion that determines the appropriate pattern in
the first place. King and Stansfields 1984 definition was phrased almost as neatly by
H. F. Osborn in 1896:
During the enormously long period of time in which habits induced ontogenic variations, it is
possible for natural selection to work very slowly and gradually upon predispositions to useful
correlated variations, and thus what are primarily ontogenic variations become slowly apparent as
phylogenic variations or congenital characters of the race.47
Osborn gave the hypothetical example of a human infant raised in a tree, where its
propensity for clutching and turning in its feet might be enhanced, and ultimately
become genetically fixed. As it happens, the males of some tribes in S. America are
virtually raised in trees, where they do all of their hunting, and their ability to clutch
the trunks with their turned-in feet and distorted big toes is quite striking. If female
tribe members and infants who do not hunt were also found to have unusual feet, it
would indicate that the feature has been genetically assimilated.48
In The Descent of Man (1871), Charles Darwin cited Alcide DOrbignys account of
exceptionally large lung capacities among the natives of the high plateau of Peru.
DOrbigny had also somehow discovered that the alveoli of their lungs were larger and
more numerous than those of the dwellers of the plains. Then Edward Forbes had
studied the Aymara, who lived at altitudes above 3,000 meters in the Andean
altoplano. They had significantly larger trunks, but shorter femur and humerus limb
bones, as well as diminutive heel projections, in comparison with lowlanders.
Subsequently Forbes encountered Aymara who had lived at low altitudes, working as
gold miners for two generations. Their anatomies were still distinct, though less
exaggerated than those of their great grandparents. Both Forbes and Darwin attributed
the bone shortening to a compensation effect for the larger trunk size. Darwin
concluded:
From these valuable observations, there can, I think, be little doubt that residence during many
generations at a great elevation tends, both directly and indirectly, to induce inherited modifica-
tions in the proportions of the body.49
There is no question that living at high altitudes has ontogenic effects such as
increased hemoglobin levels as well as expanded lung capacity. Has the effect of living
in such an environment for many generations fixed these modifications genetically?
Nowadays, possible subjects for research into human genetic assimilation are
Himalayan people, such as Tibetans or Nepalese who have been displaced to the
lowlands for several generations. In more recent studies of the ontogenic effects of
living at high altitudes, J. L. Rupert and Peter Hochachka (2001) note that while
visitors to the high Andes can accommodate to the mountain air, the local inhabitants
have a substantial advantage. And although they write that the relative contribution
of ontogenic variation and genetic adaptation has not been firmly allocated, L. P.
Greksa (1996) had previously presented Evidence of a genetic basis to the enhanced
total lung capacities of Andean Highlanders.
204 Chapter 5
Genetic assimilation was explored experimentally in fruit flies by C. H. Waddington

and his co-workers.50 If the pupae are heat-stressed, some of the adults have a
distinctive broken wing vein characteristic. A combination of continued heat
treatment and selective breeding of the flies with that phenotypic characteristic results
in a population that uniformly shows the change in venation. But this seems to be a
repression or activation of a regulatory gene involved in the epigenetic expression of
wing development. In other words, the regulatory systems were already there, some
more temperature sensitive than others. The deliberate act of selection simply sorted
out the most extreme cases. The adaptational significance of broken cross veins is
irrelevant here except in terms of the investigators requirements. In some instances of
ontogenic change in heat-stressed fruit flies, Waddington thought that the heat must
have been mutagenic, instead of latent genetic characteristics being elicited. That
comes close to defining the limit of genetic assimilation: it depends on activation of a
dormant gene or mutation of a pre-existing gene or a combination of the two.
However, a contingent novelty of gene or protein shuffling might also match the envi-
ronmentally induced change. Since natural selection does not recognize the difference
between a phenocopy caused by the environment and a genocopy established by
genetic fixation, the latter has to have a little more selective value before it becomes
part of dynamic stability. The universal existence of heat-shock genes, and their
translation to proteins that have protective and regulatory effects, is now widely
known, and they may affect evolvability. Stress proteins is their alternative name,
since a variety of physicochemical factors in addition to heat may be involved. Under
normal conditions they contribute to the formation of the three-dimensional
structure of proteins, but under stress they are otherwise engaged, and mutability
increases. (See my next chapter.)
Some of the processes discussed in the previous paragraph would come under West-
Eberhards term genetic accommodation. Her commentary on the general properties
of genetic accommodation is imbued with selectionspeak, but I will endeavor to
translate. She notes that genetic accommodation occurs whether a novel trait is
mutationally or environmentally induced and that simple statement, without the
accompanying selective regime, is a useful starting point.51 I agree with the idea that
the environment induces a phenotypic change to which the genotype accommodates;
and that the genotype is in a sufficient state of experimental flux that it can generate
developmental and perhaps behavioral changes. Her concept also includes the co-
adaptation or internal selection that follows emergent novelties and produces
internal organismal equilibria with low energy demands, a phenomenon that I raised
in chapter 4. The attempt to synthesize a variety of related phenomena is admirable,
provided that the relationships are real. However, it is not always easy to remember all
the special implications of a common word such as accommodation. And I have
already used the word with different shades of meaning for both physiological and
epigenetic responses. The invocation of molecular adaptability as it relates to genomic

change and environmental influence strengthens the overall concept (Kirschner and
Gerhart 2005).
For Matsuda the proximate event was the most interesting part of accommoda-
tion, i.e., ontogenic change caused by the environmental condition. Temperature and
light are common influences on the production of developmental hormones.
Nutrition is also indirectly involved. In many cases animals that enter a stressful
environment, such as marine animals invading fresh water, or fresh water animals
invading the land, make large eggs. This allows embryonization (i.e., the first stages
of the life cycle occur in the egg), and the vulnerable larvae are protected from envi-
ronmental stress. Ovoviviparity, where the egg is protected within the mother, and the
young are born as miniature adults, is another means of avoiding stress. And the next
stage is viviparity, where the developing young derive nutrition from the mother. This
has emerged independently in fish, amphibians, reptiles and mammals.52
To return to the epigenetic consequences of large eggs, secondary vitellogenesis is
often a factor. This increased yolk formation can be induced by temperature and
photoperiod changes that stimulate more synthesis of the hormone vitellogenin. In
crustaceans the hormone is mediated by light-sensitive organs in their eye stalks.
Matsuda observed that when sand-hoppersintertidal, talitrid, amphipod
crustaceansfirst invaded dry land they sought a damp environment and found it in
leaf mould, which is dark as well as damp. Darkness affects the production of light
sensitive hormones in the eye stalks, which in turn have two effects: de-inhibition of
androgenic hormone production, which results in accelerated spermatogenesis and
the development of the male secondary sexual characteristics, and inhibition of
ecdysone production. The latter suppresses the development of normal terminal
moults, resulting in a neotenous condition that has a variety of anatomical conse-
quences in several species of these talitrids, including the loss of the swimming legs,
and alteration of leg, antennal, and gill structure. That these changes can be brought
about by experimental manipulation of extant intertidal amphipod species supports
the hypothesis. Some of the changes in the terrestrial talitrids have, however, been
genetically fixed. The behavior of transitional talitrids seeking damp, dark places is
part of the proximate process. How they got further up the shore in the first place was
put down by Matsuda as the result of sudden changes in the level of the sea or land
or possibly mass migration. In my experience intertidal amphipods, when removed
from their normal environment, usually try to head downhill toward the sea. I was
once called by a bewildered neighbor who could not understand why shrimps were
spontaneously generating in his cats water dish. On investigation, I found a pile of
seaweed in his compost heap, from which a host of the amphipods had headed
downhill, to be channeled into a cul-de-sac at his back door, where the water dish
must have presented a refuge of last resort for the frustrated crustaceans. Death by
206 Chapter 5
dilution had turned them shrimp-pink. On the other hand, my colleague Tom
Reimchen has observed that in Haida Gwaii (Queen Charlotte Archipelago) in British
Columbia, some talitrids migrate en masse up from the shore and overwinter in grasses
above the high tide mark.53 This area was also subject to large-scale regressions and
transgressions of seawater levels when the last glacial period came to a close in the late
Pleistocene, and continuing into the early Holocene, about 12,0008,000 years ago.
Environmental stimuli may have ontogenic consequences that are coincidentally
advantageous. The polymorphism of shell markings and color in land snails provided
a classical problem for neo-Darwinism. How could such striking differences in banding
patterns and colors all be adaptational? In the common land snail Cepaea nemoralis,
which in France is a popular escargot, the background color can be green, yellow or
pink, and the black banding may be absent, or very narrow, or so wide that the shell
appears almost uniformly black. The original investigations by Arthur Cain and Philip
Sheppard (1950, 1954) inferred that the different color morphs were adapted to local
microenvironments. (The term morph can refer to color, color pattern, anatomical
structure and size.) They came at the reverse of the problem by analyzing the remains
around thrush anvilsstones that the gastronomic birds used to break open their
snails. The thrushes most commonly caught the type that was most visually
conspicuous in the local microenvironment. So the investigators concluded that the
mosaic of different environmental conditions, such as dark woods, open areas, long
grass, and short grass, had disrupted the selection process and produced polymor-
phism. But how is it you find non-adaptational coloration? In Donegal, in northwest
Ireland, I have noticed that the pink color of Cepaea makes it stand out in the seashore
grass from many yards awayplenty of potential anvils, but no thrushes perhaps?
And to what extent is or was the microenvironment directly responsible for these
differences? If a similar snail, Helix aspersa, is raised in the dark, it has a dark shell; if
raised in occasional light, it has a paler colored shell. The ontogenic effect of the light
stimulus coincidentally proffers advantageous protective coloration in both cases, and
natural selection, even as a post hoc cause is redundant. To what extent does Cepaea
respond ontogenically to its microenvironment? No one will bother to look if they
find the disruptive selection story adequate. Several unrelated species of marine snails
show similar polymorphism. I have on my desk a jar of the shells of marine gastropod
Nerita chamaeleon. They were all collected from the same square meter of sandy shore
on Kat O Chow in China. Yet the shells vary far more in color and banding patterns
than do those of Cepaea. And from the Jervis Inlet area of New South Wales I have a
vial of top-shells that are as varied as mixed humbugs in their colors and stripes. Thus,
striking polymorphisms of no adaptational significance may arise de luxe in uniform
environments.
Cor van der Weele cites a number of cases of environmental induction in her Images
of Development (1999). Caterpillars of the moth Nemoria arizona change color
according to their diet. In the spring they eat oak catkins and are catkin colored. Later
hatching caterpillars eat oak leaves and take on the color of the twigs of the tree; it all
depends on the amount of tannin in the diet. Changing photoperiod determines
whether a light or dark morph is produced in the comma moth. Araschnia levana is a
butterfly that comes in different color and pattern morphs, one of which, to add to
adaptationist confusion, looks like a map of Europe. Which morph develops in
Araschnia depends on the wetness of the climate. Ambient temperature at the end of
the larval stage determines the presence or absence of eye spots on the wings of
Bicyclus butterflies in Malawi.54 The same author gives examples of other groups
including mollusks and vertebrates where diet and physical stimuli cause developmen-
tal change. Some of these effects come down to a few facultative phenotypic options
that were genetically fixed in the past, so they exemplify the action of environmental
switches affecting existing genotypes. Others are like the color of leaf-eating caterpil-
lars. To take an example from my own research field, marine biology, dog whelks may
be white if they eat barnacles, brown if they eat mussels, or banded brown and white
if they eat both. No doubt they have been assigned selection coefficients that
explained the differences. The fact remains that the morphs were caused by the
environment, would have happened regardless of selective value, and only secondarily
were demographically distributed according to degrees of predation.
Stuart Newman and Gerd Mller (2000) add the following examples of environmen-
tal character determination. Candida albicans, known to sufferers of this fungal
infection as thrush, varies according to its environment from single cells, or
budding strings like yeasts, to septated filaments. And they have no default
morphology.55 Incubation temperatures determine sex in reptiles: high temperatures
produce male lizards and crocodiles, but female tortoises.56 Embryos of a strain of mice
that normally have five lumbar vertebrae develop six vertebrae if transplanted to the
uterus of a surrogate mother with six.57
Evolutionary epigenetics are often treated as if their emergences were autonomous,
or intrinsic, all to do with progressive, internal complexification without regard to the
larger environment. Quests for unifying physical principles that will explain complex-
ification at all levels fall into this category, as do structuralistic analyses. Cor van der
Weele believes that the internalist/structuralist position in evolutionary developmen-
tal studies abandons too much ground to ecological adaptationism, and favors
enlarging epigenetics to emphasize environmental factors. But it had already been
attempted by Matsudas synthesis of a neo-Lamarckist antithesis with a neo-Darwinist
thesis. He put the environment as a causal agent back where it belongs: in and around
the organism. Eugene Balon also transcends simplistic structuralism to view ontogenic
emergences as optional responses to new environmental exigencies.58 He points out
that there are critical stages in the life cycles of animals where there is more than one
direction to choose from. Out of these choices come environmentally cued, facultative
208 Chapter 5
phenotypic expressions. The final result may be a change of direction in development,

with the old phenotype lost through disuse. The radical reculer pour mieux sauter
regression to larva followed by a new line of hypermorphosis has taken such a route,
and in a number of cases either the paedomorphic type or the old mature adult form
can be induced. Balons work will be addressed more fully in chapter 8.
Another aspect of environmental influence on epigenetics requires attention. Mae-
Wan Ho (1984) has taken a particular interest in the significance of phenocopying,
whereby the environment can bring about ontogenic, or phenotypic changes that
mimic those produced by particular genotypes. The phenomenon was detailed by
Richard Goldschmidt (1940), and subsequently Peter Medawar (1951) came up with
the complementary term genocopying to signify the genetic assimilation of an envi-
ronmentally induced phenotypic condition. Ho is convinced that the universality of
phenocopying indicates that it is a common prelude to evolutionary change.
Reinvestigating some of the earlier genetic assimilation experiments she concludes
that the continued amplification of phenotypic effects from one generation to the
next cannot be fully explained by the modification of regulatory genes nor the
mutation of structural genes. She therefore proposes that phenocopying is mediated
by the ultrastructure of the cytoplasm, and that environmentally induced cytoplasmic
changes can persist through the egg to the next generation, to be amplified if the envi-
ronmental conditions persist.
Susan Oyama also understands the need to accommodate non-DNA influences both
within the cell and whole organism, and to bring environmental influences into the
causal interactions. In The Ontogeny of Information (1985), she writes:
What we are moving towards is a conception of a developmental system, not as the reading off
of a preexisting code, but as a complex of interacting influences, some inside the organisms skin,
some external to it, and including its ecological niche in all its spatial and temporal aspects,
many of which are typically passed on in reproduction because they are in some way tied to the
organisms (or its conspecifics) activities or characteristics or because they are stable features of
the general environment. It is in this ontogenetic crucible that form appears and is transformed,
not because it is immanent in some interactants and nourished by others, or because some inter-
actants select from a range of forms present in others, but because any form is created by the
precise activity of the system.59
Oyama goes on to conclude that the genome can explain neither epigenesis nor the
causation of epigenetic change, any more than physics can explain the nature or
change of the genome. Since Oyamas book first appeared in 1985, molecular biology
has made major inroads into epigenetics. The actions of Hox genes have created
enormous interest, and given epigenetics a scientific respectability that it previously
lacked. At the same time, molecular biology has pulled epigenetics into a tight
genocentric orbit. Only in the last few years have the kinds of eco-evo-devo studies
and assessments that support Oyamas original position been forthcomingsee, for
example, Hall, Pearson, and Mller 2003.
In my next chapter, I will enlarge on the significance of other studies of non-DNA

epigenetic events, and also summarize the advances that have been made in molecular
epigenetics and their significance for evolutionary developmental biology. I omit most
of them from this general chapter to keep the broader issues simple. But when we turn
to epigenetic mechanisms it will be more obvious that Ho and Oyama belong to a
historical tradition of dissent that has quite strong ties with neo-Lamarckism. As
Walter Garstang remarked, Ontogeny does not recapitulate phylogeny, it creates it.60
And the title of neo-Lamarckist F. Wood Joness 1943 book Habit and Heritage speaks
for itself. When I began this work I was well aware of how the environment influences
physiological change. But I was still biased in favor of autonomous emergences that
gave organisms the opportunity to undertake new experiments in behavior through
improved adaptability. In the conventional sense they allowed the organism to better
persist in its own being in a greater variety of environments. Gradually it dawned
on me how the organisms actions determine what is adaptive in the conventional
sense. Although they dont call it genetic assimilation, Stuart Newman and Gerd
Mller (2000) improve on the idea in their essay Epigenetic mechanisms of character
origination. They put it as follows:
The close mapping between genotype and morphological phenotype in many contemporary
metazoans has led to the general notion that the evolution of organismal form is a direct
consequence of evolving genetic programs. In contrast to this view, we propose that the present
relationship between genes and form is a highly derived condition, a product of evolution rather
than its precondition. Prior to the biochemical canalization of developmental pathways, and the
stabilization of phenotypes, interaction of multicellular organisms with their physicochemical
environments dictated a many-to-many mapping between genomes and forms. These forms
would have been generated by epigenetic mechanisms: initially physical processes characteristic
of condensed, chemically active materials, and later conditional, inductive interactions among
the organisms constituent tissues. This concept, that epigenetic mechanisms are the generative
agents of morphological character origination, helps to explain findings that are difficult to
reconcile with the standard neo-Darwinian model, e.g., the burst of body plans in the early
Cambrian, the origins of morphological innovation, homology, and rapid change of form. Our
concept entails a new interpretation of the relationship between genes and biological form.61
Thus, Newman and Mller take us out of the genocentric interpretation of

autonomous emergence. There the organism simply gets an interesting innovation
through genetic mutation or shuffling, and then figures out something useful to do
with itin other words, function following form. In contrast Newman and Mller
place us in a realm where extrinsic causes modulate intrinsic self-assembly
mechanisms. Behavior and the direct impact of the environment determine what is
adaptive, and what specialized adaptations will then arise. They do not however
present it as an either-or choice of intrinsic or extrinsic. And before we get too excited
I have to remind myself, and you, that these evolutionary processes depend on the
210 Chapter 5
organism having the constituent tissues capable of responding to later conditional,

inductive interactions. Newman and Mller do not miss this point. But, to them, it
is based on an inevitable feature of the viscoelastic cell aggregates that constituted the
first multicellular organisms.62 Superficially, that might seem hylozoic, and it
underrates the physiological and behavioral adaptabilities that took metazoa into new
environments in the first place.
In addition to focusing on the pre-Mendelian evolution of body plans in simple
plastic metazoans, Newman and Mller also scrutinize the final consequence: mor-
phological adaptation, which is popularly identified with evolution. We are
mesmerized by the evolution of whales from hippopotamus-like creatures, by the
massive predatory dinosaur Tyrannosaurus rex, and by Cretaceous crocodiles that were
big enough to have him for lunch. Clearly, their evolution is squarely in the
epigenetics arena. But we might forget that progressive evolution of physiological and
behavioral adaptabilities made them possible. And in emphasizing that, we should not
lose track of how physiogenesis and epigenetic changes contributed to further physi-
ological evolution. (Physiogenesis, as I have to keep reminding my physiology
students, even at the end of the course, is the imposition of physicochemical change
by the environment on the organismthe expression came originally from E. D.
Cope. And while I am temporarily digressing to deal with definitions, I should point
out that, like Lvtrup, Balon, and me, Newman and Mller use the broadest definition
of epigenetics as anything that affects development and its evolution. They not only
include non-heritable mechanisms and processes, but give them primary importance.)
We will take the origination of body plans and adaptational forms into account in
the next section of this chapter. But, before we continue, Newman and Mllers theme
is worth re-emphasis: simple, primitive, multicellular organisms were more plastic,
and responsive to epigenetic influences than complex organisms with mechanisms
that buffer morphogenesis and homeostasis. Epigenetic causes were not gene
determined, but were physiogenic, and thus contingentthey may or may not have
acted; it depended on the circumstances. Consistent behaviors and contingencies
would have led to consistently altered morphogenesis, and only then would the
linkage between phenotype and genotype be established. Then the genome would
have been able to co-opt the morphological outcome of development. Ontogeny does
not recapitulate phylogeny, it creates it. Thus, they conclude that evolvability, at least in
terms of large innovations like the emergence of different body forms decreases with
time. Genetic determination obstructs it.
Its a pattern that keeps repeating itself. For example, from a primitive behavioral
plasticity, insects and birds have evolved distinctive, genetically-fixed behavioral
patterns. The argument is logical and can be demonstrated with tangible examples. It
parallels, but gives a stronger evolutionary tone to Waddingtons image of the
epigenetic landscape. The ball rolls down the hillside, bouncing from rut to rut, but
finally canalized in a deep channel at the bottom. But this reduction of primitive
evolvability can be accompanied by the kind of evolvability that comes with increased
complexity and adaptability. That is a general feature of progressive vertebrate
evolution, something that Waddington recognized as an escape from canalization.
Birds may have become less evolvable behaviorally, but physiological and
behavioral adaptability in lineages of the placental mammals allowed radical
experiments in morphogenesis. Moreover, the jack-of-all-trades qualifications of
hominids allowed them to escape genetic co-option of behavior.
Reaching a Better Understanding of Developmental Evolution
In this chapter I have taken a roughly chronological approach to the history of general
concepts of developmental evolution, with occasional sallies into some of the better
known mechanisms. We know little enough about epigenetics in living organisms, far
less fossil organisms, or unrecorded missing links, if such ever existed. Therefore it is
difficult to begin with aboriginal unicellular organisms and provide a comprehensive
history of epigenetic evolution. To seek to construct such a history is a worthy goal.
Yet some of my students dont agree. They are indifferent to historical musings about
the course of epigenetic evolution, and to their errors and digressions. And they are
skeptical about speculation and theorizing based on inadequate data. Just give us the
factsand the textbook page numbers!
One approach would completely satisfy them. First, work out the developmental
processes and epigenetic mechanisms of a single organism. Then, to understand evo-
lutionary change, construct hypotheses that could be empirically tested by modifying
the molecular and cellular mechanisms of epigenesis in the fully understood
organism. Hence I recommend to them Walter Gehrings Master Control Genes in
Development and Evolution: The Homeobox Story (1998), which also provides a bonus
educative insight into the nature of scientific discovery. Despite my doubts about
genocentrism, homeotic gene function has provided one of the greatest success stories
in modern evolutionary studies. (See the following chapter.) Yet it also illustrates the
limitations of gene analysis for understanding evolution.
More to the point, Gehring makes frequent reference to one of the best exemples of
my students ideal, the work of Sidney Brenner and his associates on the tiny
nematode worm Caenorhabditis elegans.63 It has about 20,000 genes, and 1,000 cells at
maturity, and the invariant course of development of every cell from the fertilized egg
has been accounted for. But as Gehring readily points out, the fate of every cell
depends on the fates of other cells, and only a few of the determining factors in the
cytoplasm of particular cells have been identified. In the development of the worms
vulva the role of every cellinduction, inhibition, backup, or other supporting roles
has been discovered. The number of inducing molecular signals has been
212 Chapter 5
determined.64 But at the time of Gehrings review only two genes and their protein
products involved in epigenesis had been identified. And those genes no doubt have
a number of other essential intergenic effects.
The very success of research into cell fates in C. elegans underlines the difficulty of
understanding the role of genetic and cellular interactions in development. Gehrings
remarks concerning the determination of eyes in Drosophila also reinforces the nature
of the problem. One of the key genes for eye development in the fruit fly is paradox-
ically called eyelessit originally referred to a mutant condition. The gene has been
found to be a homologue of others that help to determine the eyes of mammals,
mollusks, and flatworms. Discovery of the Gene For the Eye! is the kind of
newspaper headline that greets findings of this nature. But there are other genes for
eyesabout 2,500 of them in Drosophila, by Gehrings account.65 The surprising
conclusion of this research is that eyes, or at least the fundamental mechanisms of eye-
development, may have emerged only once, regardless of whether they stopped at the
simple eye spot stage, or diverged and progressed to camera eyes, or compound eyes.
Previously, many biologists, including myself, had agreed with Ernst Mayr that eyes
could have evolved independently about 40 times. Hence, if it were all that likely, it
could hardly be all that difficult, and Darwins worry about the evolution of such
complex structures could be assuaged. Now all we have to do is to figure out the
smallest number of exons or whole genes that could interact with each other, together
with the smallest number of cells that need to be organized in a functional sequence
to affect differential gene expression and determine the final complex product. The
epistemological lesson, dear students, is that to progress in such understanding we
have to stagger from speculation to hypothesis, and to experiment. Then, when we
find that we cannot go there from here, we have get lucky, or lurch back to more
speculation about alternative routes.
Development and the Progressive Evolution of Complexity

Explanations of the earliest origins of organisms that undergo differentiation and
integration during their development lie partly in the causal arena of symbiosis. I have
already touched upon the emergence of eukaryotes, and then sexual and multicellular
associations, in chapter 4. At that point epigenesis became seriously involved with
evolution, although some signatures of the next level of emergence are discernable in
eukaryotic unicells, as will be seen in the next chapter.
Multicellularity
Let us return briefly to early fundamental concepts of differentiation. Erasmus Darwin
and Herbert Spencer had intuitions that a primordial filament or a unicell was subject
to differential physicochemical stimuli. Before they assembled themselves in multicel-
lular units, the unicellular progenitors of metazoa already had the contractile
microtubular filaments needed for locomotion. They also had cell surface molecules
that could hang on to a physical substrate as well as other cells. Even simple protein
stickiness, modulated by the ionic content of the environment or the cytoplasm, is
enough to account for the earliest stages of multicellularity.66 The differentiating
effects of form were increased as soon as a three-dimensional structure was achieved.
Some of the processes that form gastrular stages in metazoan developmental evolution
could simply have been differential adhesion.67 Thus, the lack of rigid genetic control
of surface protein adhesiveness provided for plasticity of form that was initially
determined by non-heritable epigenetic conditions.
If the first multicellular organisms were merely one-cell-thick mats, they could have
had some differential adhesion, and they were subject to different influences on top
and underneath, and except at the margins each cell was surrounded for the first time
by other cells. Or the first multicells may be represented by the ediacarans of the
Vendian period, which in all probability had phototrophic, chemotrophic or mixed
symbioses.
Mark McMenamin (1998) has proposed that the vendiobionts were derived from
protoctists and consisted of multicellular forms dictated by the number of cell types
in the founding organism, which would range from one to four. Each embryonic stem
cell gave rise to semi-autonomous cell families. Thus, there were one to four lineages
which cohered to one another but lacked gap junctions or a fluid-filled body cavity
that would have allowed sufficient intercellular communication for the activities of
the cell families to be coordinated. A collagenous glycoprotein coat around the cells
could have provided enough of a sticky, durable material for organismal integrity, and
to allow their ultimate fossilization. McMenamin infers an asexual budding process,
each embryo containing each of the different cell types. His hypothesis provides
grounds for explaining not only the different forms, but also their taxonomy. In a
broader theoretical sense it also explores how nature first tentatively experimented
with multicellularity, and how hopeful monsters could diversify in the absence of
competition and predation, and what limitations are imposed by lack of intercellular
communication and sharing of resources. But predation was about to come, from the
emergent wave of Eumetazoa with hungry habits.
The first eumetazoan may simply have been a sessile mat that had finally overcome
the limitations of the vendiobionts by acquiring gap junctions between the cells.
Those would have immediately have improved intercellular cooperation. Conceivably
such an organism could have had the same kinds of symbiotic nutrition as the
ediacarans. It could have sat still, absorbing particulate matter that settled on its upper
surface, or it might have crept over bottom substrates, browsing on biofilms, its
ventral surface specialized for phagocytosis. A blastula-like ball of cells might be the
next step after a sessile mat, being a physically stable configuration for a single layer
of cells released from a flat surface. But how would such an organism make a living?
214 Chapter 5
Blastulae have an independent existence as the early embryonic stages of many

marine larvae, but they are non-feeding, and possibly cenogenetic novelties that never
existed as primitive, mature organisms. Functional spherical forms are found in
colonial flagellates like Volvox, but photosynthesis provides most of their needs and
they do not require the differentiation and integration that the simplest heterotrophs
possess. Nevertheless, a blastular structure, whose cells cohered with adhesion
molecules, and which then developed tight junctions to isolate the internal
environment, and gap junctions to allow intercellular communication, would have
had differential impact on the constituent cells. Willmer (1960) showed that some
protists may have ciliated or amoeboid forms depending on the ionic conditions of
their environment. And the ubiquitous presence of ion pumps, already possessed by
unicells, resulted in ionic differences between the interior space and the outside
environment of a simple blastula. Goodwin (1989) raises these points with reference
to the basic conundrum of how organized multicellular organisms ever came into
existence:
One of the most significant steps in the emergence of greater organismic complexity was the evo-
lutionary origin of gastrulation. The transformation of a hollow ball of cells into a multilayered
structure, with the consequent combinatorial potential for reciprocal inductive interactions
leading to divers patterns of cell differentiation, stands out as a major event in the evolution of
the metazoa.68
To make a living, the blastuloid organism could have flattened out over the substrate,
continuing to feed as did the ancestral mat, with only the ventral layer specialized for
deposit feeding. Adhesion in the constituent cells is polarized, i.e., parts of them stick
easily to other cells and other parts remain free to be motile. The polarization makes
it easier to form internal compartments.69 Cells that received the largest share of food
might have grown differentially, causing the invagination of part of the ventral surface
to create a simple gut, the endoderm of the future, with dorsal cells migrating to the
interior as the mesoderm of the future. The planktonic blastula could have been an
emergent cenogenetic addition to the life cycle that would enhance its dispersal as
well as providing a new threshold for epigenetic divergence.
A potential for epigenetic differentiation already existed in the cytoplasmic hetero-
geneity of unicells. A significant role for gradients of concentration of
morphogensbicoid proteinsin the zygote and early embryo was pinpointed by
Christiane Nsslein-Volhard and Eric Wieschaus in 1980, and effectively developed by
Nsslein-Volhards 1996 Scientific American essay Gradients That Organize Embryo
Development. Her generalizations on the importance of gradients are as follows:
Some morphogenetic gradients apparently yield but a single effect: if the concentration of the
morphogen in a particular place is above a critical threshold, a target gene is activated: otherwise
it is not. In other cases different concentrations of morphogen elicit different responses, and it is
this type of gradient that is most important for providing an increase in the complexity of the
developing organism.
Although each morphogenetic gradient seems to control only a few target genes directly, inter-
actions between co-factor moleculars that affect transcription can radically change responses to
the gradients. These mechanisms of combinatorial regulation open the way to the formation of
patterns of great complexity from an initially simple system.70
Nsslein-Volhard catapults us forward in time to where her research organism

Drosophila has a morphological complexity far in advance of the blastula stage that we
are examining. But between the heterogeneous unicell and the complex differentiated
metazoan such gradients existed, and became important factors in epigenetic
evolution.
Appropriate conditions for multicellular morphogenesis came from the blastuloid
structure, which originally formed a dynamically stable configuration mechanically,
rather than by naturally selected genetic instructions. This does not entirely get over
the problem raised by Buss (1987) to the effect that a ball of ciliated cells would have
had the problem of not being able to undergo cell division, so could not reproduce.
But, any cells that intruded into the interior of the blastuloid, and were subjected to a
different ionic environment, might not have developed cilia, but would have been
available as stem cells for regeneration, reproduction and new experiments in
evolution. And when the blastuloid emerged spontaneously, inner migration of cells
could have been instantaneous. The Ediacaran fauna were possibly the first wave of
relatively simple blastuloids, although, according to Seilacher and his co-workers
(1998), there is fossil evidence for more advanced triploblastic embryos during the
Vendian. I agree with them that the diversification of triploblastic body plans could
have been rapid, however, it does not follow that it proceeded immediately.
Newman and Mller (2000) clarify the contrast between Darwinist and emergentist
interpretations:
A novel implication of this interpretation of the burst of forms during the early history of
metazoan life is that the disparate organismal forms would have been achieved with no
requirement for competition or differential fitness. Since function would follow form, rather
than the other way around, the pre-Mendelian world would thus also have been, in this sense
alone, a pre-Darwinian one.71
However, the presence of competition, even from Vendian quiltazoids, could seriously
obstruct their diversification. It is certainly unnecessary to invoke the non-
explanation of selection-pressure-for-gastrulation to satisfy the need to maintain
locomotion and reproduction. Also, as an erstwhile digestive physiologist, I find it odd
that theoreticians so easily ignore the maxim that an army (of cells in this case)
marches on its stomach.
Brian Goodwin had already attributed a large part of the process of gastrulation to
its inherent physical stability which parallels the attractors of the non-living systems
216 Chapter 5
that chaos theoreticians study. Although non-living systems do not have the
biological ion pumps necessary to Willmers explanation, the carrier proteins of such
mechanisms have a self-assembly component as well as essential biological
components, including the primary structure of the proteins, the enzyme that
energizes the system and the biosynthesized fuel molecules. That the blastular internal
milieu is ionically distinct from the outside environment is due to a combination of
mechanical and biological properties. Goodwin saves his case by noting that while he
is trying to find reductive explanations for complex systems, all levels of organization
have to be taken into account in understanding ontogeny.
Body Plans
The evolution of body plans is an essential part of the history of developmental
evolution, but I do not have the morphospace to explore it thoroughly here. I will take
it up in a future work that will go more thoroughly into evolutionary history as seen
from an emergentist perspective. In the meantime, Rudolf Raffs The Shape of Life
(1996) and Wallace Arthurs Origin of Animal Body Plans (1997) provide adequate
accounts.
Although the distinctive body plans of the marine animal phyla may have appeared
very rapidly in the early Cambrian, their tenacious stability has depended largely on
the establishment of strongly canalized homeorhesis. But along with it came some
reduction of evolvability. Even the simple anatomies of polyps and flatworms have
been canalized to the point of intransigence. Paradoxically, although it took longer for
the basic fishy vertebrate plan to emerge, vertebrate developmental evolution kept on
progressing in fits and starts for more than 400 million years, while most Cambrian
animals, with the other obvious exception of arthropods and the lesser example of
mollusks, stayed stuck in the mud.
This supports Brian Halls (1999b) contention that the neural crest is a major
generative condition for the emergence of vertebrates and their continued evolution.
This distinctive embryonic ectodermal structure appeared early in the craniate lineage.
Before it appeared, some migratory cells, especially the neuroblasts, helped to modify
body plan. But the evolutionary versatility of the neural crest justifies Halls claim that
it is an emergent, fourth germ layer. Along with duplications of the whole genome in
the early vertebrates, and further duplication and differentiation of genes that regulate
development and physiology, the neural crest provided powerful experimental tools
for emergent evolution. During the evolution of fish, amphibians and reptiles there
were anatomical experiments, often involving numbers of vertebrae, the limb trans-
position early noted by Goodrich, and the arrangement of fin-rays and digits. Among
the reptiles, for example, contrast the forms of turtles, plesiosaurs, ichthyosaurs,
dinosaurs, pterosaurs, and snakes. These could be generated by changes in homeotic
gene expression. They could also be effected by changes in cellular interactions, such
as the migration of neural crest cells, and by heterochronic shifts. But behavior must
also have been important in determining what changes would be relevant to the
animals way of life.
This version of vertebrate evolution receives some support from Newman and
Mllers view of epigenetics in the later Darwinian phase, when genetic assimilation
had resulted in consistent trueness to type. But again they point to a continuing role
for physical, particularly biomechanical epigenetic influences, even after the genome
had co-opted anatomical determination. Morphogenesis is basically a process of
organizing the embryos differentiated cells and their secretions into a variety of
shapes, such as rods, balls, and tubes with various degrees of rigidity or flexibility.
These then have a feedback effect on gene expression. For example, a migrating neural
crest cell might encounter a new obstacle. At that point it could stop and change its
usual role. Or it could go round the obstacle and induce a new set of cells to change
their differentiation. It doesnt stop there, because changes in its surroundings will
again alter the final morphogenic goal of the neural crest cell. But neural crest cells,
despite their striking epigenetic role, are not the be-all and end-all of vertebrate
epigenesis. Skeletons can be built because of the ability of mesenchymal cells to group
together and make cartilage. In a developing limb the shape of the skeleton is
determined by various interacting factors. These include spatial constraints, and dif-
ferential cellular adhesions that are modulated by the differential expression of genes.
Diffusible chemical growth stimulants and inhibitors can induce periodicities that
generate the pattern of repeated cartilages and bones found in digits and spinal
columns.72
When the foundation of a skeleton has been laid, biomechanical stimuli are
produced by the contraction of the rudimentary muscles. They consistently affect the
shape and operation of joints, and influence innervation, and vascularization. In
addition to participating in normal skeletogenesis, the ability of connective tissues
and tendons to form cartilage and bone in response to mechanical stimuli can
generate novelty. Mesenchyme cells in tissue culture are known to arrange themselves
along stress fields. Depending on the density of its cells, mesenchyme will make
cartilage under the influence of stretch and compression. Emergent structures that
come from such interactions include a variety of sesamoid bones. There are genes for
the structural proteins, growth factors and enzymes that participate in bone and
cartilage synthesis. But there is no gene-for-sesamoids. While they are ultimately
integrated into the skeleton their generation is initiated by the mechanical stimuli of
embryonic movement. Several examples are known from bird embryology.73 The
novel sail battens found in the wings of the fossil flying reptile Coelurosauravus
jaekeli probably resulted from spontaneous bone formation in the pattern of folds
generated by the movements of the embryos before they hatched from their egg.74
Although these prominent wing-stiffeners are only known from a single species, there
218 Chapter 5
is a universal bone unique to pterosaurs, the putatively sesamoid pteroid bone. It

extends from the wrist region toward the shoulder, but is not a digit. Most of the
leading edge of the wing is made rigid by the extended fourth finger, but between the
shoulder and the wrist there is only the wing membrane. Thus, the pteroid bone
probably enhanced the aerodynamic quality of the wing by eliminating flutter in a
region of the wing especially crucial in the giants Pteranodon and Quetzalocatlus that
had wing spans of up to 12 meters.
The existence of analogous structures that do the same thing in organisms with no
close phylogenetic relationship can arise from the fundamental properties of
mesenchymal tissues to respond in the same way to the same mechanical stimuli.
Anatomical homologies that do indicate phylogenetic relationship were recognized as
evidence for evolution by the nature philosophers of the eighteenth century, long
before Darwin incorporated the concept into his historical theory. The perennial
example is the vertebrate forelimb, which diversified into a variety of legs, wings,
flukes, spades, and hands, all with the same underlying anatomical pattern.
In combination with the deep homology of homeotic genes, generic epigenetic
processes, (i.e. those that respond to physicochemical effects in the same way,
regardless of phylogenetic closeness) originally produced both analogues and
homologues. Various recent theoreticians, especially in their contributions to
Homology (1994), edited by Brian Hall, have recognized that here lies one of the
fundamental secrets of evolution. Again, Newman and Mller have run the furthest
with the idea. They propose that once the extrinsic causes of morphogenesis were
genetically assimilated these Mendelian organisms became more determinate in
their epigenesis. The goals of what Waddington called creodes became more fixed,
and reliable dynamically structural modules led to the diversification of homologues.75
These gene-based functional-morphological patterns became more important than the
original generic extrinsic causes. Newman and Mller write:
This means that although homologues may first arise by the same epigenetic processes that
produce homoplasies [analogues], they eventually become independent of their underlying
molecular, epigenetic, and generic constituents and increasingly play an organizational role in
morphological evolution. They take on a life of their own and are thus inherited as structural units of
morphological organization, not tied to any particular generative process. Homoplasies reflect the
origin of morphological innovation in the generic material properties of tissuesthey are an
echo of the pre-Mendelian world. Homologues, in contrast, act as formal attractors of design,
around which more design is added.76
I have italicized a sentence here to bring out its relevance to emergence. Homologues
are new patterns with new rules of action that are consistent with the underlying rules
of genetic determination and response to physicochemical changes. But they have a
new emergent property: they take on a life of their own. The epigenesis of vertebrate
forelimb homologues does not follow an identical algorithm in all instances. The same
goal can be achieved by a diversity of routes, even in phylogenetically close organisms.
Closing Note on Evolvability

While genetic determination may have supplanted in large part the former exclusive
role of generic epigenetic causes, homologues had a life of their own. An increasingly
sophisticated physiological adaptability both buffered the experiments that they could
try, and permitted new behaviors that would encourage them to succeed. With the
emergence of mammals, the numbers of vertebrae had been reduced, their propor-
tional allocation to the spinal regions made consistent, and limb positions relatively
fixed. Like most other mammals, humans and giraffes have the same number of neck
bones. But this anatomical stability did not limit evolvability, which could continue
to experiment with allometric growth shifts and accommodations. In their early
evolution, mammals were also exploring how far their new emergent physiological
adaptabilities could take them. This had a bootstrapping evolutionary relationship
with their development, allowing them to try out habitats and new ways of living that
had previously been off limits. It was humans who were the most adventurous.
The Story So Far
I conclude this discussion of development and evolution with a summary of the sig-
nificance of embryonic change and the problems of developmental escape from
homeorhesis or epigenetic stasis, together with some recapitulatory remarks about the
physiological and associative arenas. This, along with the following chapters
summary and the completion of the field-trip checklist in chapter 7, is a preamble to
chapter 8.
1. Before the developmental evolution of multicellular organisms, cellular complexifi-

cation was achieved by endosymbiosis and the sexual association of eukaryotic
unicells, followed by primitive experiments in multicellularity.
2. Once the foundational multicellular association had formed and emerged to the
level of complexity of a gastruloid, developmental evolution became possible. It
initially involved differential adhesion, and experiments with body spaces, and simple
structural patterns that were responses to extrinsic and intrinsic epigenetic stimuli.
Ultimately epigenesis came to involve genes and their regulation. This was then made
more variable by repetitive differentiation of molecules and cell types, coupled with
reorganization, integration and regression.
3. Epigenetic algorithm is easier to say than to understand. If this, then that

depends on the environmental circumstances (this) as much as the differential
responses of the genome (that). Moreover, the genome cannot contain the
algorithmic program. Epigenesis depends on interactions between this and that.
220 Chapter 5
4. Developmental changes result in diversity of form, and affect the physiology of the
mature organism by the alteration of existing cell lineages or organ systems, or the
emergence of new ones.
5. Developmental/physiological emergences are often multifunctional, which may be

overlooked if only key innovations are sought. Furthermore, in additional to several
immediately useful emergent properties there may be features that will increase the
evolvability of the lineage.
6. Modification of existing organ systems involves heterochrony and allometric

growth shifts that may have a component of genetic drive that causes change in a
particular direction, regardless of fitness. This being the case, then the heresy of ortho-
genesis needs to be resurrected as a legitimate embryogenic concept.
7. When basic body plans of the animal phyla were constructed in the early Cambrian,
homeorhesis was weak. They did not all necessarily originate simultaneously, but they
all took off at the same time, due to the weakness of competition and predation.
Natural experiments that resulted in successful emergent body plans are best placed
on a time scale commensurate with the duration of the life cycles of simple marine
animals, rather than on a geological time scale.
8. Internal selection or physiological coadaptation over geological time has established

developmental dynamic stability (= homeorhesis). This constraint on body plans has
occasionally been surmounted by animals that remained confined to the marine
environment, such as crustaceans, mollusks and primitive fish.
9. Emergence from the sea to fresh water and terrestrial environments initiated
progress in the developmental evolution of plants, and provided direct environmen-
tal effects on the epigenesis, and mature physiology of animals. These were then
internalized in varying degrees by genetic assimilation. More flexible behavior
increased the feedback between environment, physiology and development.
10. Although homeorhesis affects terrestrial animals and plants, there have been
enough environmental disequilibrating effects to induce or encourage experiments in
evolutionary progress to greater complexity, and enough related disruptions of
ecostasis to help establish novel emergents.
11. Bursts of diversification of successful emergents accompany the relaxation of

natural selection:
a. in the wake of catastrophe.
b. in the invasion of pristine environments.

c. on the re-invasion of old environments after a period of progressive evolution in
new ones (e.g. teleosts returning to the sea).
12. Lamarck was right about the importance of the individual, and the way it can
affect evolution by its behavioral choices. As evolution progresses, the freedom of
choice increases exponentially, which further affects epigenetic and physiological
evolution.
13. The neo-Lamarckists were right about the importance of the direct effect of the
environment on the individual, and evolutionary consequences.
14. There are numerous ways in which an organism can break away from firmly
established developmental patterns:
a. Simple regression to a juvenile form that often works well in association with
symbionts, or hosts, in the case of parasites.
b. Regression to an early stage, and development from there in a non-traditional
direction (= reculer pour mieux sauter).
c. Cenogenesis, i.e., insertion of a diversionary life cycle stage such as a butterfly
caterpillar, while coming back on line to terminate in the typical adult form.
d. Hypermorphosisadding on to the end of epigenesisaffects both anatomy and
physiology.
e. Early diversion of normal development by a particular creode or cell line that is
internally integrated and also accommodated (ontogenically buffered) by other
developing lines. Sometimes this is caused by the insertion of temporary interphenes
that may be atavistic or novel (= key epigenetic innovations). This is the process most
likely to create the unlikely, or to produce saltatory novelty.
f. Metamorphic phases or thresholds in life cycles that are affected by environmental
conditions increase the likelihood of developmental change.
15. The conservative nature of the genes that contribute to foundational epigenetic
functional units (or holons, or modules), such as homeotic gene clusters and key
organizing embryonic cells, partly explains the tenacity of homology, in addition to
parallel evolution and aspects of convergent evolution. Their repetitive differentiation
also allows them to be repatterned with highly diverse phenotypic consequences.
16. But there exists an emergent property of homology that cannot be reduced to
genes and their differential expression. And long after a developmental role had been
established for the genes, there persisted responses to intrinsic physicochemical
causes, and extrinsic environmental causes.
222 Chapter 5
17. These effects resulted from the behavioral activity of animals. Physiological adapt-
ability. not only permitted behavioral changes, it also helped to buffer developmental
novelties.
18. Some extrinsic biotic causes (symbionts sensu lato) have had persistent and
prolonged effects on development that have very little to do with genetic determina-
tion.
6
Epigenetic Mechanisms
Some genetic structures do not adapt the organism to the environment. Instead they have
evolved to promote and direct the process of evolution.
J. H. Campbell, 19851
In pan-environmentalism, environment consists of both morphogenetic and selective factors. It

is envisaged that the former induces, by response of the genotype, variation upon which the
selective factor(s) work. It follows, then, that there will be appreciable evolution with environ-
mental changes. (Conversely, there will be no appreciable evolution without environmental
change.)
Ryuichi Matsuda, 19872
. . . the present relationship between genes and form is a highly derived condition, a product of
evolution rather than its precondition. . . . [The concept] that epigenetic mechanisms are the
generative agents of morphological character origination, helps to explain findings that are
difficult to reconcile with the standard neo-Darwinian model, e.g., the burst of body plans in the
early Cambrian, the origins of morphological innovation, homology, and rapid change of form.
Stuart Newman and Gerd Mller, 20003
Since much of the information in the structural genome is shared by all organisms,
from bacteria to humans, the explanation of differences among organisms has to be
sought, in part, in genetic structures . . . that promote and direct evolution. These
include mechanisms that affect mutability, and regulate differential gene expression.
To operate, some mechanisms of evolution at the genome level require spare parts,
such as the junk DNA components that constitute about 75 percent of some
eukaryotic genomes.
Geneticists classify anything involving DNA as genetic, and define epigenetic
processes as those heritable regulatory mechanisms that also involve DNA. But this is
too genocentric. The DNA keys of the genetic keyboard are necessary if the music is to
be played, but they are neither player nor score. Suppose that conventional wisdom
were true: the developmental instructions for any organism are in its DNA. Lets
further suppose that the DNA can initiate protein synthesis all by itself, and
224 Chapter 6
everything goes from there. We are already in the Looking Glass World at this point;
but even if what we saw in there were real, we still would not understand how it could
have evolved to make different organisms.
Isnt mutation of the genes, and natural selection enough? cries a student who
wants it to be simple. I tell him that reduction to the genes leaves out the organism,
its actions, its environment, and its evolutionary history. Environment was a large part
of that history, and although it is a large part of selection theory as well, we should be
more interested in the environment as a generator of evolutionary novelties, than as
a selective eliminator of them. Furthermore, although organismal and environmental
factors can be reduced to the molecular and physical levels, they cannot be induced
from those, since they involve physiology, behavior, environmental changes, and all
of their interactionshe was sorry he asked.
Because of the phenomenal and causal complexities, I do not limit epigenetics to
heritable features, but prefer Sren Lvtrups broad definition of epigenetics as encom-
passing anything that affects the course of development, along with his inference that
anything that changes the course of development causes evolution (Lvtrup 1974).
Two of the epigraphs for this chapter were chosen to emphasize how environment
initiates epigenetic change; because it is a general principle that must not be forgotten.
However, this chapter focuses largely on the molecular and cellular levels.
In 1913, Jakob von Uexkll proposed that Mendelian elements must be regulated by
supergenes: a hierarchy of control must be involved in evolutionary change. Richard
Goldschmidt also realized that changes in the genes could neither explain speciation,
nor the large epigenetic changes that might generate hopeful monsters. The Material
Basis of Evolution (1940) proposed that chromosome mutations and their consequent
position effects altered epigenesis. Stimulated by Goldschmidts theory, Barbara
McClintock discovered position effects in corn genetics in the 1950s. They did not
result from chromosome mutations, but were the effect of small, transposable
elements that caused changes in gene expression when they jumped from one
chromosome to another. They are not necessarily beneficial, but provided that their
effects are harmonious, and that the integrity of the developing organism is not
compromised, such natural experiments may continue until a hopeful monster
emerges. Position effects are important at the ultrastructural chromatid level since
interacting segments of DNA have to be in the same place at the same time. We could
also say that position effects are caused at the cellular level by the influence of
adjacent cells.
While McClintocks research was getting under way, Franois Jacob and Jacques
Monod were investigating the bacterial lac operon, the first mechanism of gene
regulation to be worked out at the molecular level. Their discoveries excited the same
Cold Spring Harbor molecular biologists who had treated McClintock to blank looks.
But although the lac operon became well known, its theoretical relevance to evolu-
Epigenetic Mechanisms 225
tionary epigenetics, though suspected by its authors, was largely ignored as a special
case of bacterial function.
Epigenetics and its associated vocabulary were not elaborated until C. H.
Waddington published The Strategy of the Genes (1957). Though well received, it lacked
mechanistic detail that might explain how gene strategies were effected or altered.
Subsequently, Lvtrups Epigenetics (1974) was a valiant attempt to marshal the
biochemical evidence for evolutionary epigenetic change. Conceptually persuasive to
some readers, its molecular database was insufficient to fuel a paradigm shift. Due to
technical difficulties, and the hostility of the Modern Synthesis to epigenetics and
other relatives of the hopeful monster, it was not tried and found wanting, but found
difficult and not tried.4
In Phenotypes (1994), David Rollo remarks that although persuasive molecular
evidence for developmental evolution did not accumulate appreciably until the 1980s
it was time for the focus of evolutionary thinking to be shifted to epigenetics, and that
is how things have gone in the last decade. Wallace Arthur comes at the subject from
the same background of evolutionary ecology, and his The Origin of Animal Body Plans
(1997), makes a similar recommendation. A rich lode of epigenetic molecular
biological evidence from current literature is Epigenetic Inheritance and Evolution (1995)
by Eva Jablonka and Marion Lamb, who admit to a Lamarckist bias that I will come
back to consider at the end of the chapter. Fundamentals of Molecular Evolution (1991;
second edition, 1999), by Li Wen-Hsiung and Dan Graur is a good general source.
Cells, Embryos, and Evolution by John Gerhart and Marc Kirschner (1997) has the same
fin-de-sicle resonance as William Batesons 1894 Materials for the Study of Variation. For
anyone who wants the full degree program, Scott Gilberts Developmental Biology
(1997) is not only the most encyclopedic presentation of the information that I
examine in this chapter, it also pays some attention to its history and its more
provocative implications. Brian Halls Evolutionary Developmental Biology (second
edition, 1999) is another comprehensive treatment of epigenetics in the context of the
Modern Synthesis, and also explores its historical roots. Mary Jane West-Eberhards
Developmental Plasticity and Evolution (2003) takes the subject beyond mere evolution-
ary epigenetics to the point where it stretches the Modern Synthesis to the limits of its
plasticity. Lynn Caporales Darwin in the Genome (2002), does not focus on epigenetics,
but has serious implications for it, and is a rich source of information regarding
genomic mechanisms that have evolved to promote and direct the process of
evolution as Campbells epigraph puts it.
Marc Kirschner and John Gerharts 2005 book The Plausibility of Life: Resolving
Darwins Dilemma provides the most recent and comprehensible synopsis of epigenetic
ideas, but it entangles them almost inextricably with neo-Darwinism. Eva Jablonka
and Marion Lambs Evolution in Four Dimensions: Genetic, Epigenetic, Behavioral and
Symbolic Variation in the History of Life is more accessible to the general reader than
226 Chapter 6
their 1995 opus, but although they are familiar with some of the escape routes they
are still trapped in the hand of Darwin.
To grasp the difficulty of understanding molecular evolutionary epigenetics,
consider one of the advertised goals of the human genome project. At the outset, it
claimed it would be able to provide a clearer understanding of human evolution, as if
this would automatically result from accurate knowledge of all the base sequences of
the genome. However, to understand evolution we would also need to know what the
genes do, discover all the proteins for which they code, and how the proteins
function, and how all of these interact. And all this would not solve the more
refractory problems of physiology and behavior and associated environmental effects.
Moreover, to understand the evolutionary significance of human base sequences
alone, we would also need similar information about, say, the genome of the
chimpanzee, and a number of other organismal types going back through the line of
evolution of the vertebrates and their ancestors. Even so, the well-known genomes of
bacteria, yeast, roundworms, fruit flies, and a hundred other species are proving to be
almost as relevant to evolution as those of our close relatives. They are an invaluable
repository of information necessary for the thorough establishment of phylogenetic
relationships, and they relate how base sequences have changed in relation to evolu-
tionary diversification. However, information about the regulation of gene expression
is more valuable to evolutionary theory than a genomic encyclopedia.
In scale, the largest genetic differences between us and our closest cousin, Pan, the
chimpanzee, are chromosomal inversions and translocations. These repositionings
and novel combinations of chromosomal segments may be partly responsible for
some of the phenotypic differences that we can see, but may simply be random
changes that contributed to mutual sterility before or after the divergence of our lines.
The genomes, at the level of structural gene content, are virtually identical. The
putative 1.3 percent difference is just as great within the human species as it is
between us and the chimpanzees. In fact there is a huge overlap between the genetic
constitutions of all living species, in terms of their abilities to make structural proteins
and enzymes. All organisms have the same building blocks of DNA and protein. It is
how they arrange and use those building blocksto make a simple cell, or to make a
complex, multicellular humanthat is important.
Think of the basic genome as a pantry full of ingredients.5 A Chinese chef and a
French chef might go inside, take out very similar arrays of items, and produce two
totally different meals. Similarly, epigenetic recipes produce two distinct organisms by
combining the same basic ingredients in different ways and by allocating different
seasonings and cooking times. If we have comparative information about how genes
are expressed during embryonic development, in quantity, in quality, in rate, and in
concert, we have an important key to understanding the fundamental evolutionary
mechanisms that make organisms so diverse. To contribute some kind of answer to
that problem, this chapter will survey molecular mechanisms that relate to morpho-
genesis and epigenetic evolution.
Neo-Darwinism was satisfied that random point mutations of the structural DNA
that codes for proteins were sufficient raw material for the operation of natural
selection. To a degree this is indeed sufficient for simple, though inflexible, adaptation
to environment. Yet epigenetic evolution could progress without the accumulation of
such point mutations, through alterations in mechanisms of gene expression. A con-
ventional response is this: It doesnt really matter whether it is mutations of
structural DNA or regulator genes. So long as they happen at random, natural selection
will sort them and so gradually direct both simple adaptation and the increase of
complexity. I will establish in this chapter that all change at the DNA/RNA and
chromosomal levels is discontinuous, and that many such changes can be considered
saltatory, with dramatic epigenetic consequences. Through the redundancy of
repetitive DNA, experiments can be conducted in non-adaptive change, out of sight
of natural selection. Moreover, many genomic changes are non-random, and can
have a self-amplifying effect correlated with allometric morphological change, i.e.,
shifts in the anatomical proportions of organisms. Furthermore, it is possible for the
environment to effect phenotypic changes that are heritable and that persist when the
environmental influence has been removed. Some epigenetic evolution has to do with
the ultrastructure and biochemical composition of the cytoplasm of eggs. Finally, and
most heretically, as the Newman and Mller epigraph suggests, it is possible that most
early evolution was caused primarily by the interaction of the organism and its
environment, and only secondarily worked into the genome.
The introduction of technical language that will be unfamiliar to some readers is
unavoidable. Even for professional biologists the terminology is difficult because it has
grown haphazardly. Sometimes several terms are used for the same mechanisms, and
sometimes terms retained for their historical priority are thoroughly misleading. I will
keep them as simple as possible, as much for my own sake as anyone elses. Any
specialist biologists who are still with me will have to tolerate the catalogue of
elementary explanations of mechanisms and structures that are needed to make sense
of molecular epigenetics. A plain-language summary of established molecular
mechanisms of epigenesis that bear upon evolution is provided at the end of the
chapter.
Modifications of Gene Structure
The best-known process conventionally associated with evolution is non-synonymous

base substitution through point mutation. This automatically results in an amino-acid
substitution in the protein for which the DNA codes, once the transcription and
translation of the code through RNA intermediates have been completed. Ever since
228 Chapter 6
the point mutation was first understood, it was taken to be a random process. This is
now questioned by Lynn Caporale (2003). She cites, for example, mechanisms that
increase hypermutability in particular parts of genes. In their essay Large phenotype
jumps in biomolecular evolution (2004), F. Bardou and L. Jaeger model the effects of
mutation on biopolymer folding (i.e. tertiary structure). They find three categories of
point mutation: 1. Those largely lethal mutations that cause extreme changes in
structure; 2. Those that cause moderate changes with phenotypically significant and
non-lethal effects; 3. Those that have minimal effect that might allow for fine
tuning of an existing system. Their model fitted the effects of 157 point mutations of
a ribozyme. As to randomness, the majority of actual point mutations were in category
2, and so, there is some quality of the genome that makes them non-random. Bardou
and Jaeger also postulate that large phenotype jumps are possible in this system,
especially involving category 1 under environmental stress. None of these events are
cumulative adaptational processes directed by natural selection.
Eukaryotic genes contain exons, which have the structural genetic code, and
introns, which are spacer components that are not translated into protein structure.
However, they facilitate shuffling of the sequence of exons, and that does have an
effect on protein structure. Gene structure can also be changed by intragenic recombi-
nation, that may reduce part of the DNA structure of a chromatid, or add to it, or
simply mix parental chromosomal characteristics. I will refer to some of these
processes in further detail below.
DNA Modifiers of Gene Expression
Prokaryotic Mechanisms
The lac operon system has no direct bearing on eukaryotic epigenetics, but it is
familiar to most biology students and is a useful introduction to the vocabulary
needed to address the genetic components, and their products and interactions. It also
illustrates how distinct strains of prokaryotes can be established by cytoplasmic
inheritance, which is important for epigenetics in multicellular organisms. The system
is an array of genes that controls the output of the enzyme -galactosidase in
Escherichia coli, a common bacterium of the human gut. The structural gene, which
codes for the relevant enzymatic protein, is part of the lac operon complex. Two other
structural genes in the complex make permease, which gets the lactose into the
bacterial cell, and transacetylase, which acetylates unusable galactosides before their
elimination from the cell. The three structural genes are physically together on the
same strand of DNA, accompanied by a DNA switch called an operator. The operator
is adjacent to a DNA promoter sequence, which allows the enzyme RNA polymerase
to begin to transcribe the structural genes to make messenger RNA. If the operator
switch is off the transcription does not take place and the enzymes are not
synthesized. The enzymes are not often needed anyway, so the switch is usually off.
Alongside the operator there is a regulator gene that codes for a repressor
protein, whose presence in the cell locks the operator in the off position. For the lac
operon to be activated fully, two conditions have to be met: lactose has to be available,
and glucose, the energy source most commonly used by E. coli, has to be absent. If
lactose is in the cell, some of it spontaneously converts into the isomer allolactose,
which combines with the repressor molecule, inactivates it, and thereby unlocks the
operon, allowing the ultimate synthesis of the necessary enzymes. However, if glucose
is also abundant in the bacterial cell there is a scarcity of cyclic AMP, which is needed
to make the lac operon promoter more receptive to RNA polymerase. The cyclic AMP
(cAMP) combines with catabolite activator protein (CAP) to stimulate the expression
of the lac operon structural genes. Therefore, the production of the lac operon
enzymes can be inhibited and stimulated by separate systems.
Two different strains of E. coli can arise in media containing lactose. Its uptake is
stimulated in cells that have some permease. In others that lack permease to begin
with, there is no uptake of lactose to trigger the production of the galactosidase. When
cells that have permease reproduce, their daughter cells have enough of the enzyme
already in the cytoplasm for them to continue to use lactose. Thus, cytoplasmic
inheritance of the appropriate protein molecule determines the action of the strain in
the next generation, although both the strains have identical DNA.6 The bacterial
control of gene expression shows how well tuned and responsive cellular homeostasis
is in the most primitive kind of organism.
Eukaryotic Mechanisms
Knowing that such a regulatory system existed in bacteria led to a search for similar
systems in eukaryotes, but because gene structure and regulatory systems in
eukaryotes proved to be much more elusive and complex than the operons of E. coli
there was no rush to embrace their implications for epigenetic evolution. One problem
arose with the discovery that the genes that need to be called into use simultaneously
for a coordinated biochemical pathway are often found on non-homologous
chromosomes, and each has its own promoter. This required some mechanism, such
as a common sequence responsive to a common triggering substrate, capable of
making all their promoters say go at the same time. Moreover, some promotor
sequences are complex algorithmic switches that probably evolved by the repetition
of simple DNA holons, which then differentiated to become responsive to a variety of
activating molecules.
The nomenclature for genes that influence the expression of the structural genes
varies somewhat throughout the literature. Among the choices available, modifier
genes and regulators signify the most general category of DNA sequences that affect
230 Chapter 6
gene expression, and related molecular mechanisms. These fall into several categories.
Replicators mark the spots that begin and end DNA replication; recombinators
mark recognition sites for recombination enzymes involved in phenomena such as
crossing over, transposition events, increases in exon shuffling, and gene duplications.
Segregators are DNA sites where chromosomes attach during mitosis and meiosis,
before they are pulled apart to enter the new daughter cells. Promoters, along with
sequences called enhancers, are attachment sites for inhibitor or activator
molecules, and switches for DNA transcription. The promoters respond to proteins
synthesized in the nucleus. In some cases they bind proteins synthesized in the
cytoplasm. These are activated by steroid hormones, upon which they enter the
nucleus and affect specific promoter sequences. The activation of promoters demon-
strates how nuclear proteins, cytoplasmic proteins, steroids from the extracellular
milieu, whole organism physiological cycles, and environmental cycles may all be
influential in regulating structural gene activity.
In addition to structural genes that code for structural proteins and enzymes, there
are many structural genes that code for regulatory proteins, including selectors such
as Hox and Pax-6 genes involved in appendage and eye development respectively.
Others code for enzymes involved in DNA and RNA transcription; RNA modification;
DNA repair; DNA acetylation and methylation; recombination, and the synthesis of
non-protein activators or inhibitors such as cyclic AMP and steroid hormones.
Products of this kind are also important in regulating organ function in multicellular
plants and animals. Finally there are the genes that code for DNA packaging, and
binding proteins such as histones. Codon, exon and gene duplications, transpositions
and point mutations of any of these genes could have an epigenetic and hence evolu-
tionary impact. Some authors use developmental gene as a catch-all term for any
modifier or structural gene involved in epigenesis.
Regulatory Role of RNA

RNA interference can silence gene expression, either via direct interaction with DNA
(transcriptional gene silencingTGS), or by interactions with other RNAs (post-tran-
scriptional gene silencingPTGS). Predominantly a homology-driven means of
associating with other nucleic acids, interference RNAs (iRNAs) can recruit
methylation machinery to genomic sites. RNA can prevent the expression of genes by
interfering with the translation of mRNA into protein. This involves single-strand or
double-strand RNA molecules binding to a genes RNA transcript, in essence silencing
that transcript. Occurring universally in plants and animals, micro-RNA molecules
(miRNAs) interfere with messenger RNAs (mRNAs) by directing their cleavage by
RNAase. Because of their small size, about 22 bases in length, miRNAs long evaded
detection.7
Thus, a genes ability to speak can be muzzled, preventing translators from making
sense of the words, or the spoken word can be snatched before it is heardcertain
RNA molecules have the ability to completely alter gene expression without any
change in the genome sequence.8
Role of Steroids
Steroids are molecules whose synthesis occurs by the activation of synthetases,
proteins whose own synthesis requires a DNA code. Therefore changes in the code,
and hence the structure of the synthetases can effect alterations in the steroids that are
produced. In addition to regulatory proteins, steroids affect enhancement sites and
activate mRNA transcription. In multicellular animals, steroids originate in endocrine
glands and are passed by simple diffusion or in the blood circulation. Their presence
is often activated by environmental conditions. More than 40 years ago, the insect
steroid ecdysone was known to change the chromosome puffs in Drosophila polytene
chromosomes, because these could be seen under a light microscope. The presence of
messenger RNA could be detected histochemically by radioisotope labeling.9 Some
vertebrate steroid hormones and other hormones inactivate a protein repressor and
release the positive action of the enhancement sites for structural gene transcription.
Thus, the duplication and variation of the genes for steroids and other nuclear
receptors contribute to cellular differentiation and growth during development. Their
repetitive differentiation has also played an important part in reproductive physiology
and the evolution of homeostasis. Hormones involved in gametogenesis, yolk
deposition, metabolic rate, excretion, salt and water balance, calcium regulation,
peroxisome proliferation, the elaboration of visual pigments and other functions all
require differentiated nuclear receptors. The emergence of the vertebrates has been
linked with the doubling and redoubling of the entire genome. This had multifunc-
tional potential, because now four copies of the original primitive steroid receptors,
and all other genes, were then available for differentiation.10
Some regulatory genes have several promoters, making it possible for them to be
transcribed by various activator molecules a number of times during cell differentia-
tion, an arrangement that may modify the products of the regulatory gene as well. It
is also likely that regulatory proteins interact with each other as well as with DNA
recognition sites involved in gene transcription. The co-existence of all of these
regulatory mechanisms presents a wide range of possible combinations that are
needed for a sophisticated differentiation hierarchy of regulatory levels. From these,
large-scale or small-scale evolutionary changes can emerge.
Mechanisms That Introduce Genomic Variability

Point mutation substitutions, part of the process of protein alteration, were once taken
to have the miraculous power of providing any molecular variations demanded by
selection pressure. Ever since it became possible to work out the primary amino acid
sequences of proteins, it has been known that many substitutions have occurred
232 Chapter 6
during evolutionary history, and it was inferred by selectionists that these were all
adaptive, though there is now wide support for the view that many are simply neutral
and persisted through genetic drift. Many beneficial point mutations involve
duplicated genes, which contribute to an adaptability that gives the organism choices
appropriate to conditions. Beyond change in the DNA of the genes, there are the kinds
of epigenetic controls of gene expression that have just been outlined. But we have not
yet done with events that increase variability at the gene level.
Exons and Introns

Exons are the bits of the eukaryote gene that are ultimately translated into protein, but
in eukaryotes they are separated by intron sequences that are initially transcribed into
messenger RNA and then pruned out before translation, so that their DNA code
normally has no influence on the structure of the protein that is synthesized. Self-
splicing introns are found in bacteriophages, and protozoa, as well as chloroplasts, and
mitochondria. From the genes of the latter they were introduced into the eukaryotic
nuclear genome, and spread by the actions of transposable elements called
retroposons, which are described below. The self-splicing function of these introns
was replaced in the nuclear translation apparatus by spliceosomes. These are
complexes of small RNA molecules and proteins capable of editing newly synthesized
RNAs, and altering these templates for protein synthesis via translational start and
stop sites. Alternative splicing permits the generation of numerous proteins from a
single gene transcript.11 Histone genes have no introns, but some structural genes
consist mostly of introns that may widely separate exons from one another. All of the
DNA in exons and introns may be subject to repetition through non-conservative
DNA replication and repair mechanisms.
After initial transcription there are steps, over and above silencing mechanisms, that
can still affect gene expression before it is finally translated into polypeptides, and
afterwards, during the construction of the final protein product from the polypep-
tides. Large proteins may be assembled from polypeptides produced by several
separate coding sequences. Since each of the coding sequences consists of exons
interrupted by introns there is a potential for gene repatterning through intragenic
recombinationthe crossover occurs in mid-gene, resulting in the production of
modified polypeptides and therefore different proteins. With the discovery of introns
it was quickly realized that gene exons could be shuffled to make new genes, which
would enhance genetic variability. Exon shuffling could provide for evolutionary
experiments through random differentiation of the resultant proteins, and there is
evidence for such rearrangements.12 For example, the differentiation of genes for
cellular adhesion proteins results in the wider differentiation of tissues.
Exons can be deleted, duplicated and translocated. Furthermore, novel genes may
be generated by involving introns in protein synthesis instead of having them excised
from the messenger RNA. This involves mutation in the splicing instructions to cause
the intron to be read as an exon, which is known to occur in Drosophila epigenesis.13
A more dramatic differentiating effect may be achieved by overprinting, whereby
existing base sequences are read in a new frame, with the result that a new gene
arises from the overlapping of two adjacent old genes that still retain their original
functions.14 Introns also have a role in the regulation of gene expression.15 That might
in part be why eukaryotes, which have introns, have greater evolvability than
prokaryotes, which lack them.
Protein Domains
The significance of exon shuffling points to the next higher level in the hierarchy of
the cell, namely the proteomic level. Large proteins consist of a number of
domains (distinct units with structural or functional roles). In different combina-
tions they account for the larger variety of proteins. An annotation of the draft human
genome sequence included a comparison of protein domain types from several
organisms. Protein collections obtained for yeast, nematode, fruit fly, and human
contained 3,136, 9,254, 8,896, and 15,312 proteins, respectively. This indicated 973,
1,183, 1,218, and 1,865 domain types.16 But the number of genes, in the tens of
thousands for most higher eukaryotes (approximately 30,000 in humans), is far greater
than the number of different protein domains. Some domains may involve several
amino acid sequences brought into functional relationship by the three-dimensional
structure of the protein. In other words, such functional domains are not
determined by a particular gene, but by several genes, or by particular exons of several
genes. We cannot understand them in terms of genomic information alone, since the
epigenetics of protein complexification adds greater meaning. Thus, it seems likely
that the more fundamental relationship is not between the numbers of genes and
proteins, but between the number of possible protein domains and the original
number of primitive exons. It is exon shuffling, duplication, and insertion, in addition
to intron co-opting, and intron insertion and deletion, that have built up the more
familiar variety of genes and proteinsand made repetitive differentiation possible at
the molecular level. Another active participant in genomic shuffling is the intron that
is not merely a meaningless partitioning segment, but can code for endonucleases,
splicing directions, and other elements that affect RNA structure and protein
synthesis.17
Nevertheless, the genome can still inform us about protein structural domains
whose primary amino acid sequence conforms to the sequence of exons in a particular
gene. A good example of a functional change brought about within the gene by exon
duplication is cited by Graur and Li (2000). In the guts of most animals, chy-
motrypsinogen is activated to become protein-digesting chymotrypsin. In the
Antarctic cod, Dissostichus mawsoni, the gene for this endopeptidase was duplicated.
234 Chapter 6
An original chymotrypsinogen gene was retained for digestive functions. But in the
other copy, exon duplication and mutation, as well as incorporation of some intron
sequences, turned out an antifreeze glycoprotein. There is a self-amplifying
component in glycoprotein production as well since often a large protein with
repeated tripeptide segments is cleaved to produce many antifreeze molecules.
Logsdon and Doolittle (1997) attribute this to a strong positive selection pressure
brought about by climatic change when Antarctica froze between 5 and 14 MYA. This
textbook example of the power of the metaphor of selection pressure should be a
cautionary tale for those who combine selectionism with molecular biology.
An alternative explanation does not draw upon a metaphorical force, and it puts the
molecular information in a wider context. Repetitive differentiation, which had
previously produced trypsinogen and chymotrypsinogen from a common gene
ancestor, now resulted in another molecule that added to the adaptability of the fish
it could penetrate colder water with new food resources and fewer predators. Not only
were competition and predation diminished in that environment, the cod population
there would be largely composed of the strain with the antifreeze. It was the behavior
of the cod that determined both the demographic and genetic consequences. What the
organism does determines what is advantageous. The drop in temperature need not in this
case have epigenetically triggered an increase in antifreeze synthesis, but that too
deserves consideration. The more adaptable the organism, the greater the freedom to
conduct and test evolutionary experiments. And those experiments depend upon the
availability of components that are not adaptive but redundant.
Repair Mechanisms
Since the operation of repair mechanisms has more to do with cellular homeostasis
than evolutionary change, it is their failure that is involved in epigenetic experiments.
It has long been common knowledge that high-energy radiation (including x rays and
ultraviolet light), and many chemical environmental factors, are mutagenic and car-
cinogenic, and organisms are in constant danger of these influences to themselves and
their offspring. But there are ways of repairing damaged DNA. In his extended
metaphor of natural genetic engineering, James Shapiro (1992) calls this quality
control.
A wide range of enzymes exists for this purpose. For example, radiation has the
common effect of covalently bonding adjacent thymine bases into dimers that cannot
participate in DNA transcription. The affected triplets can be excised by a repair
mechanism, and the gap filled by the action of DNA polymerase and ligase. The
accidental chemical conversion of cytosine to uracil is corrected by a specific enzyme,
and there are also enzymes that proofread and correct DNA strands during replication,
such as 3'-5' exonuclease and a component of DNA polymerase III. Mutation of the
DNA sequence that codes for this component causes a great increase in the mutability
of the affected organism. There is also an inducible SOS system (as in the Morse code
for help) that responds to radiation injury, both repairing the faults and stopping
mitosis until the corrections are complete. However, the operation of the SOS process
can also increase mutability.18
When breaks in DNA are detected, the cell usually shuts down until such time as
the break is either repaired, or the cell enters into programmed cell death (apoptosis),
a key feature of multi-cellular organisms that maintains overall organismal integrity.
There are two general pathways by which DNA breaks can be repaired: homologous
recombination (HR) and non-homologous end joining (NHEJ).19 The first involves
copying of homologous template sequences, to ensure the proper replacement of any
lost sequences, but can lead to errors in crossing over or gene conversion events
(discussed below). The second class of repair (NHEJ) is via direct religation of broken
ends, which usually leads to little or no change in DNA sequence but can produce
translocations or gross chromosomal rearrangements. Left unrepaired, these kinds
of damage would most likely have a negative effect on epigenesis. However, there
are other kinds of DNA alteration that could change the course of epigenesis,
and repair mechanisms are part of the apparatus of canalization. Therefore any
decrease in the effectiveness of repair could contribute to epigenetic change by
loosening canalization.
Heat-Shock Proteins
At the molecular level, all organisms are capable of mounting a response to physico-
chemical and biotic stresses. A highly conserved group of heat-shock proteins (HSPs)
normally assist other proteins in folding (conformational changein some cases the
HSPs are referred to as chaperonins), subcellular localization, and other cellular
homeostatic functions. Under stress, they protect the cell and repair other proteins.
Under temperature increase, exposure to oxidants, or infection, the heat-shock tran-
scription factors (HSFs) undergo conformational changes, whereby their domains are
disrupted and new sites are exposed, enabling them to bind DNA and induce the tran-
scription of heat-shock genes. These proteins act to repair other damaged proteins,
and defer the entry of the cell into apoptosis. Proteins capable of changing conforma-
tion and activating genes in response to changes in the cellular environment certainly
introduce another level of control with respect to differential expression of existing
genetic information.20
Gene Duplication
I have made much of the general process of repetitive differentiation. If a body
segment, or an organ such as a limb, or a molecule, such as an enzyme is repeated, or
duplicated, the spare copy can be modified or differentiated to complement the
existent unit, thus increasing overall adaptability. Therefore the variety of ways in
236 Chapter 6
which multiple copies of DNA and RNA can contribute to complementary changes in
gene expression deserves scrutiny.
Some kinds of repetitive sequences called satellite DNA are repeats of short
nucleotide sequences usually found in condensed chromatin, and are clustered near
the centromeres and the ends of the chromosomes. They may play a structural-
functional role as transition zones between euchromatin and heterochromatin. There
are perhaps millions of copies of some of these sequences and they may add up to 25
percent of the total DNA of the genome in some organisms. Their somewhat
misleading name is derived from the way in which they separate in an ultracentrifuge.
They are also lumped under the heading junk DNA, which is also an unfortunate
misnomer for a pool of material that probably has an important role in evolution.
Even so, the puffer fish, Fugu rubripes, has a genome that has been largely stripped of
its junk DNA, and it survives and reproduces perfectly well.21 Whether or not it has
sacrificed evolvability in so doing, it now provides a useful contrast for the interpreta-
tion of junk DNA in other species.
A kind of repetitive DNA that has attracted much attention constitutes telomere
repeats at the ends of chromosomes, which are replenished through the action of
telomerase, a specific reverse transcriptase. Telomeres are now understood to extend
the longevity of cell lines. Thus, their gradual degradation is equated with aging, since
telomerase activity seems to diminish with increasing numbers of cell divisions.
Sometimes, amplified DNA is physically separate from the chromosomes. The toad
Xenopus laevis has many copies of the gene responsible for the synthesis of ribosomal
RNA in one chromosome. Many additional copies float free in the cytoplasm of the
developing ovum. Other amphibians can get by with much fewer ribosomal RNA gene
repeats. This dose repetition or amplification guarantees the rapid synthesis of
many ribosomal RNA units needed during development, after which the extra copies
are degraded. Gene duplication that causes only dose repetition results in more of the
same product being produced faster, and is sufficient to alter development. Other
examples of dose repetition through somatic gene duplication are found in widely
different organisms. For example, groups of genes in the fruit fly responsible for laying
down the outer layer of the egg are multiplied during oogenesis.
The most controversial aspect of gene duplication is the possibility that it might be
initiated in direct response to a particular exigency. Mammalian cells in culture,
exposed to the drug methotrexate, replicate by several hundredfold the gene for the
enzyme dehydrofolate reductase, which breaks it down.22 However, there is a slight
tendency for this gene to be duplicated even in the absence of the drug. Specific
repetitions of genes for the enzyme aspartate transcarbamylase and for the metal-
detoxifying protein metallothionein-I have also been found in mammalian cell
cultures.23 These are somatic duplications that would not normally be heritable; but
there is also an example in a human family with a history of exposure to organophos-
phate insecticides. They have a hundred repetitions of a mutant gene for

cholinesterase, which confers resistance to the toxins and probably arose during sper-
matogenesis when the gene is active. In some plants, genes that proffer resistance to
herbicides are similarly multiplied.24 Could chronic exposure to such stimuli initiate
appropriate duplications in germ line cells at vulnerable developmental stages and
pass such duplications on to subsequent generations? Activity of retrotransposons
seems to peak in germ cells, suggesting that during the global rearrangements in
epigenetic patterns there is room for copying and repositioning genetic sequences
within the genome.
In a few types of animal, including nematodes and arthropods, there is
chromosome diminution or chromosome deletion (differential chromosomal loss
as cell lineages develop). This may be why August Weismann (1893) generalized
incorrectly in his Biophore Theory that cells differentiate by retaining only a small,
distinctive portion of the original genome of the zygote. Some differentiated cells lose
all of their chromosomes; for example the red blood cells of mammals are anucleate,
but they have a large enough supply of the appropriate mRNA to keep on synthesiz-
ing hemoglobin for the several weeks of cell life.
The kind of gene duplication that is particularly relevant to repetitive differentiation
occurs where there are multiple copies of the same structural or modifier gene, either
clustered on a particular chromosome, or dispersed on non-homologous
chromosomes. Duplication of these genes can occur through uneven crossing over
during the first division of meiosis, when gametes are being produced. This is one of
the least disruptive possibilities, although the gamete that loses its genes to a sibling
cell will be sterile. Particular genes in particular lineages have a tendency to be
duplicated, suggesting a built-in susceptibility for uneven crossing over at specific
chromosomal loci. This duplicative trend occurring in the same part of the genome,
rather than randomly at unpredictable points, could contribute to allometry.
Replication slippage during the synthesis of new DNA strands before mitosis and
meiosis can also duplicate DNA sequences. This is most likely to occur in DNA strands
where there is already a degree of duplication of coding sequences, so that the slippage
does not totally disrupt replication. Only short DNA sequences are affected. Repetitive
microsatellite DNA has a variety of functions in bacteria. The ability of Neisseria
gonorrhoeae to infect epithelial cells of the host is made possible by a cell surface
protein whose stickiness depends on multiple copies of a CTCTT base sequence in its
gene.25 These result from frequent replication slippage during cell reproduction. The
same errors produce CAAT base repeats in three different genes of the meningitis
bacterium Hemophilus influenzae. If present, the microsatellite repetitive DNA seems to
make the bacterium more resistant to the hosts immune system. If absent, the bacteria
are better able to invade the host. Alterations of the CAAT repetitions allow infection
first, and then resistance to immunity. Note that a single individual cannot do the
238 Chapter 6
switching. It must occur with division. However, the resulting adaptability is at the
population level. Such contingency genes have also been found to affect cell
movement, reception of environmental chemical stimuli, and resistance to
antibiotics.
In eukaryotes, a positive role for repetitive microsatellite DNA has been harder to
find. Anticipation is a condition caused by replication slippage; Huntingtons
disease and myotonic dystrophy are examples. A particular gene codon is repeatedly
amplified to the point where the gene is no longer functional. This self-amplification
process is discussed in chapter 7. David King (1994) has already pointed out that this
phenomenon could have a non-detrimental evolutionary effect of altering gene
regulation.26 And he notes that it would not only result in a rapid generation-by-
generation amplification but would also be highly mutable. Subsequently, Kings
prediction has been in part borne out by a study by John Fondon III and Harold
Gardner (2004), which is also discussed in the following chapter.
Walter Schaffners laboratory has demonstrated that microsatellite DNA for multiple
glutamines or prolines, if inserted at the beginning of a gene, would increase protein
production.27 One way of getting satellite DNA or other sequences into genes is by
means of the repair process for double strand breakages that occur quite commonly
during mitosis. Recent studies in plants, yeast, and mouse cells show that double-
strand breaks (DSBs) in DNA can infrequently be patched with other fragments of
DNA. Presumably, the same proteins which bind to broken DNA ends in the genome
will also recognize extrachromosomal DNA fragments as DSBs, and recruit them to the
repair site. This process is found in humans.28 Moreover, a report of an inherited
chromosomal translocation in mouse cells showed the insertion of a mitochondrial
DNA sequence into the breakpoint. This not only suggests that insertional repair
patching can not only affect the germ line but also effect organelle-to-nucleus gene
transfer.29
Another possible duplication mechanism is reverse transcription of messenger RNA.
DNA repeated in this manner lacks promoter sequences, but may come under the care
of a pre-existing promoter. This is another way that some of the genes of proto-mito-
chondria could have been transferred to the nuclear genome. According to Lewin
(1988) about 25 percent of the mammalian genome arose in this manner. And the
recent human genome analysis suggests that more than 50 percent of the human
genome arose from the insertion of repetitive elements.30 Reverse transcription
contradicts the central dogma that information can only flow one way, from DNA
to protein. A number of cases have been documented in which a non-transposon
mRNA had somehow recruited a reverse transcriptase enzyme and produced a cDNA
copy of itself, which has inserted elsewhere in the genome, resulting in a
pseudogene. Errors in the initial expression of retrotransposon element can also
result in a read-through event, whereby additional sequences downstream of the
element are included in the mRNA transcript. When reverse transcriptase produces a
cDNA copy of the transcript for insertion elsewhere in the genome, the original
flanking genomic sequence is carried along for the ride. Other involvements of trans-
posable elements in a separate process of gene duplication are discussed below.
Extra copies of genes are also acquired through the duplication of an entire
chromosome, or of the full assembly of chromosomes through polyploidy.
Variation of Duplicate Genes

Some duplicate genes become varied (or variant) repeats through mutation or
exon shuffling. This is the official name for repetitive differentiation at the molecular
level. These changes can produce variations on the same protein theme, or molecules
with novel functions. They are less likely to be detrimental to the organism if there are
back up copies to conduct business as usual while natural experiments on genes are
taking place. Examples of repetition and variation of the genes for hemoglobin,
protein hormones, muscle kinases and hormones involved in digestive tract and blood
sugar regulation were given in chapter 4. Of particular epigenetic interest is repetitive
differentiation of genes for hormones involved in development. Growth hormone
underwent sustained bursts of rapid modification during early stages of elasmobranch,
teleost, and amphibian evolution. Then during the diversification of placental
mammals there were similar spurts in early artiodactyl and primate diversification. An
increase in growth hormone in mice, induced by transgenesis of rat genes, results not
only in giantism but also behavioral change.31 Prolactin was derived from the same
gene family as growth hormone by repetitive differentiation. Its variant repeats
regulate salt and water in fish and amphibians, broodiness and the production of crop
milk in birds, and its most familiar function of mammalian milk production.
Duplication and differentiation of steroid hormones has been important in
development and reproduction. In addition, the systems that they regulate can be
further complexified through repetitive differentiation of their receptors. Baker (1997)
suggests that receptors for androgens, glucocorticoids, mineralocorticoids, and prog-
esterone evolved from an ancestral steroid receptor gene by two successive
duplications over a brief time that could have coincided with the origins of
vertebrates. He continues:
Moreover, the duplications of these steroid receptors may be additional evidence for the two
duplications on a genome-scale that have been proposed to be important in the evolution of
vertebrates. The two successive duplications of steroid receptor genes and their subsequent
sequence divergence leading to steroid-specific receptors that regulate growth, development,
reproduction and homeostasis in vertebrates may have been one of the events important in
vertebrate survival after the Cambrian during global extinctions that occurred about 440 and 370
million years ago.32
240 Chapter 6
The range of receptors in the repetitively differentiated molecular superfamily that

directly affects the nucleus includes those for thyroid hormones, steroids, retinoids,
peroxisomes, vitamin D, and a variety of others. Swapping of domains from different
origins was also involved.33
In addition to the simple tendency for duplications to keep affecting the same
chromosomal loci rather than being purely random, there is a mechanism called
concerted evolution that emphasizes the multiplication of particular variants.
Within a gene family that had arisen by tandem duplication, i.e., side by side on the
same chromosome, an apparent directiveness to mutational variation in the genes was
discovered. Moreover, in related species where the same gene family existed,
presumably because the common ancestral species initiated the duplication trend,
there could be a divergence of this mutational variation in a different direction.34 This
kind of mechanism could relate to divergent evolution, but if concerted evolution
continued the same trend in related clades it could contribute to parallel evolution.
Concerted evolution spreads particular mutations within gene families. The
phenomenon was first called molecular drive by Dover (1982), who saw that its
operation was independent of natural selection:
The widespread fixation of variants by molecular drive is different in that it is an outcome of a

variety of sequence exchanges within and between chromosomes that give rise to persistent non-
mendelian patterns of inheritance. Significantly, there are circumstances in which the activities
of the genomic mechanisms, in spreading sequence information between chromosomes, would
lead to the progressive increase of a variant through a family more or less simultaneously in each
individual of a sexual population. This concerted pattern of fixation by molecular drive may
provide an explanation for the origins of species discontinuities and biological novelty.35
Li and Graur add: Concerted evolution essentially means that an individual member
of a gene family does not evolve independently of the other members, a multigene
family evolves together in a concerted fashion, as a unit.36
The mechanism that brings this about is much the same as that which causes the
duplications in the first place: unequal crossing over, and a related phenomenon
called gene conversion. The processes cause reduplication within multiplied gene
families containing varied repeats. Particular variants become duplicated as a result of
concerted evolution, and the more copies of a particular variant that there are, the
greater the probability of it becoming reduplicated again and again. This trend can go
on without reference to any adaptive value of the initial duplicate genes or their
concerted evolution. Gene conversion does not increase the total number of
duplicates, only the proportion of particular variants within the gene family, so it
avoids the possible detrimental effect of dosage imbalance.37 This results from the
disequilibration of dynamic stability by competition from multiple duplicates for
scarce energetic or molecular resources.
In contrast, if, as neo-Darwinism originally assumed, mutational experiments are

random, there should be no identifiable trend except that caused by the natural
selection of adaptive variants, and both related species should show a heterogeneous
scattering of mutations, related only where selection pressures are identical. By neo-
Darwinist logic, two distinctively different kinds of selection pressure would be
needed, for such trends to diverge in two species of the same genus.
In addition to the duplication of whole genes and chromosomes, exon duplication
within a gene also occurs, and some large proteins with repetitive domains (multiple
functional regions) have originated in this way. For example, the trypsin inhibitor of
egg white is a protein with three functional domains for inhibiting trypsin and similar
serine-endopeptidases, such as chymotrypsin and bacterial subtilisin.38 This gives egg
white an antibiotic quality. The synthesis of fats involves the most multi-domain
mosaic genes that are known. Curiously, while this applies both in fungi and
mammals, the components of the genes are different, and have undergone different
evolutionary routes to converge with the same function.39
Transposable Elements
Most of this segment is drawn from Li and Graur 1991. Transposable elements can
move from their original position in a chromosome to different sites in the genome,
usually affecting gene expression in some way. The synonym jumping gene has
been bumped from the official lexicon because it is not always a gene that jumpsit
may be a bit of one or more than one. And a jump is too close to a saltation for tra-
ditionalists. A transposition may be conservative, in which case the element takes
itself to a new region of the genome, leaving a gap behind, or it may be duplicative or
replicative, leaving a copy of itself behind when it jumps. A transposable element may
also make the leap by proxy through retroposition. It is transcribed to RNA that is
then reverse-transcribed to DNA, which is inserted into a new chromosomal locus.
Transposition usually leaves a signature in the form of a direct repeat, a short
sequence duplication of the adjacent DNA.
Some transposable elements are only active in specific tissues, for example germ
cells. This is consistent with the differential availability of DNA in different tissues,
determined by methylation and histone binding. Some transposable elements always
jump to the same site, some prefer a particular chromosome, some prefer a region rich
in certain bases, and some jump randomly. Transposable elements fall into three
categories. Insertion sequences contain only enough genetic information to effect
transpositionvehicles without passengers. They are known to occur in prokaryotes,
viruses, and eukaryotes. Transposons are larger, containing genes that code for a
variety of products in addition to the information that lets them transpose. One kind
of bacterial transposon carries the genetic information for an entire bacteriophage,
including the genes that code for the protein coat and invasive enzymes of the virus.
242 Chapter 6
Retroelements or retroposons contain DNA or RNA sequences for reverse tran-

scriptase, the enzyme that causes DNA to be synthesized from an RNA template. In
mammals there are multiple copies of these, such as the long interspersed nuclear
elements (LINEs), consisting of up to 800,000 copies in humans, though the vast
majority are no longer full-length, and hence incapable of producing the machinery
necessary for further transposition. There are also short interspersed nuclear elements
(SINEs), as well as other transposons and endogenous retroviruses. Altogether, these
make up more than half of the human genome. However, it is misleading to class the
parts of the genome that do not code for proteins or constitute modifiers of gene
expression as junk DNA. Many genes have been found to contain parts of repetitive
elements, such that the most common protein domain in the human proteome is one
derived from reverse transcriptase, and the introduction of not just exons but also
introns from repetitive elements can introduce novel splice sites.
The most complex kind of retroelement is the retrovirus. The retrotranscription of
its RNA to DNA in the host cell initiates the synthesis of new viral protein and RNA
that contains the genetic information for the next generation of viruses
Retroelements produce retrogenes, which are open to copying errors and may not
be functional when inserted back into a DNA strand. In mammals there are multiple
copies of functionless retropseudogenes, the constant eruption of which has been
called Vesuvian evolution.40 Although evolution here seems somewhat of an exag-
geration, the possibility of a significant novelty arising randomly by this method
should not be overlooked.
The following are potential evolutionary epigenetic effects of jumping genes:
Transposition of genetic defenses and novelties in prokaryotes. This is in addition to

plasmid exchange through conjugation.
Enhancement of downstream gene expression on the same DNA strand. Dormant

genes may be awakened (known in yeast).
Gene activation, and inhibition.
General increase in position effects.
Potential for novel exon shuffling through the transposition of exons, introns, control
sequences, etc.
Increase in unequal crossing over, which results in gene duplication.
Gene duplication, with the potential for doubling rates of protein synthesis, with links
to allometry (or orthogenesis).
Increased mutation rate (known in E. coli and Drosophila). Gerhart and Kirschner
(1997) comment that suppressors of transposable elements could be lost through stress
or inbreeding, resulting in an active period of gene rearrangement and insertional
mutagenesis.41 (Did Hugo De Vriess condition of mutability not imply something
of the sort?)
Hybrid sterility. Hybrid dysgenesis is known from strains of Drosophila where a

group of transposable elements produce high mutation rates, chromosome breakage
and failure of gonadal development.42 A similar dysgenesis arising from feminiza-
tion of males is caused by the parasitic bacterium Wolbachia in a variety of insects and
terrestrial isopods.43 To top that, Wolbachia infection can rescue Drosophila oogenesis
made defective by mutation.44
Paedomorphosis. A simple transposition could also be responsible for paedomorpho-

sis through the inhibition of a gene coding for the synthesis of a key developmental
hormone. Transposition that causes repeated gene duplication in the same locus is
also one of the likely causes of gene duplication leading to allometric change and
orthogenesis.
Speciation. Li and Graur (1991) speculate that transposon-mediated alterations in

gene regulation could be responsible for rapid sympatric speciation.
Transgenesis. Retroviruses, the most complex form of retroelements, have long been
suggested as mechanisms for one of the most radical kinds of natural genetic
engineering experiment: transphyletic exchange of genes. One early known example
involves a virogene that was transferred from baboons to cats about 10 million years
ago. Although the number of known examples of such exchange are limited,
exhaustive searches were not made until the human genome project was completed.
Even when a transgene pops up from the genome there remains the problem of cross-
referring it to its origin, if it does not match up with existing genome data banks.
However, numerous bacterial genes have been identified in the human genome. Also,
the synthesis of salivary amylase is promoted by an exogenous retroviral segment of
DNA.45
Position effects. If operator and activator segments of DNA can be repositioned, the
variability of gene expression increases. Thus, the evolutionary epigenetic potential of
position effects, whether through chromosomal mutation or transposable elements, is
now better understood. Goldschmidt (1940) came close to the modern interpretation
when he argued that repatterning of the genes was more important than the mutation
of the genes. Many of the phenomena that have been raised here involve heritable
244 Chapter 6
change, and must have occurred in the germ line of developing organisms. Many
others occur only in specific lineages other than the germ line and are not therefore
heritable. Plants are much more likely to pass on the effects of somatic gene multipli-
cation since their cells retain totipotency and can enter the gametogenic cell lineage
at a late stage in development.
Selector Genes
Selector gene is a catch-all expression for all the genes involved in the development
of all the body compartments in the antero-posterior axis. Best known from Drosophila
research, they include segment polarity genes, terminus genes, and homeotic genes
such as Hox, Pax-6, and the Wnt group. The word selector is not intended to imply
that the genes are agents of natural selection, but rather that they are involved in the
determination of the particular pattern of development that the compartment will
undergo. Noting that a comprehensive treatment is impossible here, and that there
have been rapid advances in the last ten years, I organize this section in the manner
of Gerhart and Kirschner (1997).46 Not all molecular biologists and journals follow the
rules for gene nomenclature consistently. Specific gene names are always italicized.
Sometimes the general group name is not italicized although the first letter is
capitalized. Like many molecular biologists (and all biological taxonomists) I prefer to
italicize the genus or group name as well as the specific gene name.
Segment Polarity and Terminus Genes

In insects there are 17, 18, or 19 segments, most of which are recognizable in the
adults. Twelve segment polarity genes are involved in the development of paraseg-
mental compartments, which give rise to the mature segments, each of which retain
the same general cellular and organ architecture. Terminus genes are associated with
the anterior and posterior ends of arthropods, parts whose development is regulated
independently of segmentation. In primitive arthropod larvae the anterior end, which
is involved in the formation of the mouth and gut opening, develops very early,
allowing the microscopic planktonic animals to feed. The posterior end is specialized
as a swimming organ which is essential for planktonic existence, and also employed
very early in the life cycle. Most of the segmental development takes place after the
termini have reached a functional condition in the larvae.
Homeotic Genes
Hox
One of the most interesting discoveries in the fruit fly is the existence of highly
conserved, linearly arranged clusters of homeotic Hox selector genes, with distinctive
marker sequences called homeoboxes.47 Sometimes the physical sequence of the
genes on the chromosomes conforms to the chronological sequence of their

expression during development. They have been found in many animals, including
cnidarians, mollusks, and vertebrates, and are responsible for the anteroposterior axial
regulation of segments, or somites, and their appendages. Thus, it is in the fruit flys
Hox genes, or somewhere in the epigenetic chain of command from Hox to the final
construction of the limbs, that changes produce the classical conditions antennapedia
and bithorax, among others. In the antennapedia condition, a leg appears in place
of an antenna. In the bithorax condition, an extra thoracic segment with an extra
pair of wings appears. The polycomb gene is known to perpetuate the repressed state
of Hox genes where their action would be inappropriate, and its mutation is one of the
reasons for the homeotic macromutations just mentioned. Hox genes are not
responsible for the nuts and bolts of limb construction. They regulate segmental
construction through their protein activators and are in turn activated or locked up by
other epigenetic mechanisms.
The earliest flying insects had multiple segmentally arranged wings. There are two
theories of how they arose: as extensions of the dorsal exoskeletal plates, or as
modified legs that first functioned as gill/swimmerets in aquatic insect larvae.48 If the
winglessness of Apterygota, such as springtails and silver fish, is a primitive feature,
wings emerged later than the basic body plan. The familiar arrangement of two pairs
of wings was not primitive, but what was left after regression of an extensive
segmentally arranged set.49 Although Hox genes alone did not dictate the emergence
of wings, they are believed to be involved in the ultimate suppression of all but two
pairs of thoracic wings. Moreover, the homeotic Ubx gene suppresses the posterior pair
of wings and contributes to their modification as halteres in Diptera, such as
Drosophila.50 What is fascinating about insects is the way that homeotic genes allow so
much morphological plasticity within the rigidity of an adult body plan that basically
conforms to two antennae, four wings, and six legs arising from a similar array of body
segments.
There is a consensus that what came before the insect body plan was an arthropod
with many similar segments with legs arising from most of them, as in myriapods.
Therefore, Hox genes were expressed in most of the segments. Since the gene clusters
share deep homology with others found in the simplest unsegmented animals, they
must have remained active when segmentation emerged, and then undergone
repetitive differentiation coupled with changes in downstream phenotypic expression
to produce the varied forms of the antennae and palps and legs (and swimmerets in
crustaceans as well as gills in aquatic insect larvae).51 William McGinnis and his
colleagues have demonstrated how laboratory experiments with Hox gene expression
can reduce the number of legs in the brine shrimp Artemia.52 In terms of evolutionary
tempo, there is no other description for this kind of experimental result other than
saltatory. Once the regression of abdominal limbs in the early insect lineage
246 Chapter 6
occurred, expression of Hox was locked, resulting in adult forms that are all recogniz-
able as insects.
As De Beer (1940) emphasized, the evolutionary rigidity in the mature insect body
plan is offset by the evolutionary plasticity of the larvae. Insects of species with almost
identical adults can have quite different larvae. The most sophisticated holometabolic
insects, like the Lepidoptera, undergo a metamorphosis that effects marked changes in
form, physiology and behavior from the larvae to the adult formthe imago.
Cenogenetic phenomena involve epigenetic changes in larvaeusually referred to
as feeding adaptations or specializationsthat deviate from the ancestral type. Hox
expression in the caterpillar or maggot is different from that of the adult.
Metamorphosis in insects is not the condensed hypermorphosis found in the
development of frogs from tadpoles. Instead, once the parasegments have formed in
the holometabolic insect embryo, some clumps of cells are set aside as imaginal
discs. These grow considerably as the voraciously feeding larva develops, and then
they differentiate during pupation, obtaining additional nutrients from recycled larval
tissues. In a sense, two different organisms grow and develop out of the same genome,
providing more nutritional and behavioral flexibility during the life cycle of the whole
organism.
An intuition of the evolutionary significance of segmentation of body parts, and
their subsequent differentiation, was what gave E. D. Cope his concept of repetitive
addition. William Bateson came close behind with meristic variation, and it is intel-
lectually satisfying to see how the explanation of all of these organismal phenomena
ties in so closely with the way they are repetitively differentiated at the molecular
level. Although fruit flies with four wings, or with legs growing out of their heads, may
be hopeless monsters, the universality of Hox genes indicates that some homologies
are very ancient, conserved metazoan features. For every hopeless antennaped fruit fly,
there are all the successful monsters that emerged in the past to give rise to new phyla
and orders. Not only did Hox genes affect the arthropods, they were likely involved in
the explosive diversifications of the Cambrian as well. Calling this universal
phenomenon deep homology conveys the idea nicely.
In the vertebrates Hox genes participate in craniofacial development, hindbrain
morphogenesis, axial structure, including the anatomy of the vertebral bones, limb
arrangements and other aspects of epigenesis.53 Many of these functions are controlled
at the cellular level by the organizing effects of neural crest cells, as described in the
previous chapter. The fish-like lancet, Branchiostoma lanceolatum (formerly known as
Amphioxus), a non-vertebrate chordate, has a Hox cluster whose gene sequence
anticipates the lineup of the multiple Hox clusters of jawed fish. And primitive jawless
fish, still represented among the living by the lamprey and the hagfish, have two Hox
clusters. This signifies evolution by homeotic gene duplication, once before the
emergence of the Agnatha, and another time before the emergence of the jawed fishes,
giving the latter four clusters. (This kind of evolution might also be considered to be
orthogenetic.) In fish evolution the pectoral and pelvic fins may have emerged from
continuous lateral fins by suppression of Hox genes in most of the intervening body
somites.54 Further differentiations of the Hox genes that initiate pelvic and pectoral
fins then led first to lobe fins in the sarcopterygian ancestor, limb formation in its
tetrapod descendants, and finally regression of the number of digits to the familiar
pentamerous pattern.55 Hox participation in limb growth is independent of somite, or
vertebral number.
Wnt
The name Wnt originally signified wingless in Drosophila, which has seven variants
that, like Hox, are involved in segmental organization. Also like Hox, Wnt genes were
primitively involved in the differentiation of the antero-posterior axis, especially the
posterior end. There is one Wnt in the freshwater cnidarian Hydra. It participates in
the organization of the oral region, which is regarded as morphologically posterior. In
the deuterostome lineage they influence the development of the blastopore region.
Vertebrates may have 19 different Wnt genes, and one later evolutionary role is the
morphogenesis of the mid and hind brains. They are also partly responsible for the
early stages of organogenesis by influencing the separation of the mesoderm into the
organ rudiments called anlagen. In addition, Wnt genes interact with migrating
neural crest cells and help to induce tissue formation in the early embryo. Their
interaction with other selector genes is summarized and extensively referenced in
Schubert and Holland 2005.
Pax
Another deeply homologous homeotic gene type is the Pax-6 cluster responsible for
initiating the morphogenesis of eyes. The implantation into Drosophila of a squid Pax-
6 gene cluster causes a multiplicity of eyes to appear all over the bodies of the flys
offspringfruit fly compound eyes, not squid camera eyes, mind you.56 This riotous
result shows what can happen when genes are transferred to organisms that have no
stable regulatory mechanism for them. But from the evolutionary point of view the
more interesting point is that the lineages of squid and insects have been separate
since they diverged from their last, common, unsegmented worm ancestor in the early
Cambrian. Lacking a common ancestral organ, their eyes are non-homologous at the
organ level but deeply homologous at the level of the homeotic epigenes that trigger
their final construction.
Walter Gehring (1998) discusses the earlier bridging of an even greater phyletic gap,
namely between vertebrates and insects. Mouse eyeless is a molecular relative of Pax-6.
When transferred to the imaginal discs of larval fruit flies, they induce ectopic eyes
(i.e. eyes that arent where they ought to be) on the antennae, wings and legs. These
248 Chapter 6
transgenic eyes have normal photoreceptor cells that respond to light stimulation by
emitting an electric pulse. Gehring also makes the point that such master control
genes are not genes for eyes but are involved in eye induction along with another
2,500 genes.57 Although we now know that in animals that already have the capacity
to develop eyes, certain genes can trigger their appearance in odd places, we still have
to understand how all those genes cooperate, and how the capacity to develop eyes
arose in the first place.
On the ability of nature to experiment with eyes Gerhart and Kirschner have this to
say:
There are many more mysteries in the convergent evolution of eyes in different animals, but
perhaps none so eerie as the complex anatomy of the cubomedusan jellyfish eye in a species
without a brain. . . . The 24 eyes of this primitive jellyfish each have a lens, a cornea, a pigment
layer, and a sensory layer. . . . The existence of an eye with anatomy similar to that of vertebrates
in an animal without a central nervous system shows how far complexity of one part of function
can go without the other. If jellyfish were ever to develop a brain, they would be ready to
appreciate the world around them.58
The jellyfish does have a nervous system, and George Mackie (1999) shows that it
possesses a considerable degree of organized complexity despite its non-centralized
nature. Cubomedusan eyes have considerable resolving power and species that attach
to substrates can possibly select suitable objects for settlement. These sea wasps orient
toward light, swimming in response to the signals from the most strongly illuminated
eyes, and some can avoid objects that cast shadows or create turbulence. Higher
animals with image-forming eyes can, however, put them to a wider variety of uses
such as finding mates and prey and avoiding predators. But if there is no need or
selection pressure for these functions, can there be a selectionist explanation?
The phenomenon may instead illustrate how far natural experiment in the
epigenetic evolution of organized complexity can be taken prior to acquiring selective
value. Brian Goodwin (1994) argues that there are universal generative conditions for
the emergence of eyes in animals that include translucent epithelia, light-sensitive
neurons, and the presence in the diet of light-sensitive pigments that came from
plants that used them in photosynthesis. A range of potential crystallin proteins for
lenses occur in every cell. Pax-6 genes and their relatives that stimulate lens formation
and brain growth are common throughout the animal kingdom. And cells have
cytoskeletons whose shapes and sizes can be changed in reaction with calcium to
invaginate or bulge. Eye morphogenesis is in part triggered by simple physical forces.
Goodwin writes:
The processes involved are robust, high-probability spatial transformations of developing tissues,
not highly improbable states that depend on a precise specification of parameter values (a specific
genetic program). The latter is described by a fitness landscape with a narrow peak, correspon-
ding to a functional eye in a large space of non-functional (low-fitness) forms. Such a system is
not robust: the fitness peak will tend to melt under random genetic mutation, natural selection
being too weak a force to stabilize a genetic program that guides morphogenesis to an improbable
functional goal.59
The conventional focus on natural selection as the generator of improbable ends is

what makes Michael Behe (1996) conclude that complex structures like eyes are
irreducible, and what makes Richard Dawkins demand strict gradualism to
accommodate reducibility. For example, as cited by Behe, Dawkinss rationale is this:
Evolution is very possibly not, in actual fact, always gradual. But it must be gradual when it is
being used to explain the coming into existence of complicated, apparently designed objects, like
eyes. For if it is not gradual in these cases, it ceases to have any explanatory power at all. Without
gradualness in these cases, we are back to miracle, which is simply a synonym for the total
absence of explanation.60
Since evolution cannot be the explanation of itself, Dawkins must be really arguing
that evolution has to be gradual for natural selection to be have an adequate causal
role. In contrast, Behes irreducible structure is one whose subunits by themselves
confer no selective advantage, so they cannot be built as accumulations of
adaptations. He infers that a mutation at any step in a specific genetic program may
throw the whole process into confusion. Also, it is highly improbable that all of the
mutations necessary to produce a novel complex structure could coincide. But Behes
view is clouded by the conventional assumption that the accumulation of point
mutations is essential. The default mode need not be the miracle of intelligent
design. Goodwins mechanistic spatial-transformation model illustrates how eyes, as
highly probable robust structures, have emerged independently a number of times and
have persisted despite genetic accidents. They do not require an accumulation of point
mutations, but self-amplifying processes that have been outlined above, plus the
influence of epigenetic mechanisms involving Pax6 regulators. Autonomous complex-
ifying processes that generate eyes arise from ubiquitous generative conditions. Their
emergent transition into a more organized, and more energetically stable phase
requires no directing selection pressure. This is how Kauffman as well approaches the
emergence of complexity in The Origins of Order (1993). Furthermore, as Goodwin
argues, the robustness of the process can opportunistically take alternative routes to
reach the required form in different homologues.
Epigenesis beyond Gene Determination
In this chapter I have paid quite a lot of attention to DNA-epigenetic factors, and
relevant RNA and proteomic factors that are necessary components of epigenesis. I too
inhabit a genocentric universe, and I have not reached the escape velocity implicit in
the idea of Stuart Newman and Gerd Mller (2000) that gene modification might only
250 Chapter 6
consolidate prior epigenetic changes. But I never intended that genes be taken as the
controllers of specific epigenetic programs. To have any role they must interact with
physicochemical, ultrastructural, organismal, and environmental factors. Some of
these combinations have intriguing consequencesMarilyn Monk (1995) suggests
that throwbacks and some apparent cases of inheritance of acquired characteristics
might be due to the expression of deep homology through demethylationhence
derepressionand mutational modification of ancient ancestral motifs.
Stephen Jay Goulds 1983 essay Hens teeth and horses toes anticipated Monks
conclusions, and shows that Darwin had already thought that deep within organisms
crowds of invisible characters . . . separated by hundreds or even thousands of
generations from the present time . . . lie ready to be evolved whenever the organiza-
tion is disturbed by certain known or unknown conditions.61 The question of hens
teeth, synonymous with scarceness, arose from an experiment by Kollar and Fisher
(1980) that caused mouse mesenchyme to produce teeth, when chick gill arch
epithelium was used as an inducer. By itself the mesenchyme only synthesized spongy
bone. Chicken epithelium still has the robustness to induce tooth formation, after 60
million years of toothlessness in birds, although bird mesenchyme has lost the ability
to react to the induction. That kind of plasticity is controversial, since tradition has
carved the Use-It-Or-Lose-It Principle in stone.
Epigenetic Inheritance Systems

The term epigenetic inheritance system includes any process whereby an organism
in general, or its cell lineages in particular, follow characteristic, established lines of
development. The genome alone is not responsible for differentiationit requires a
variety of epigenetic interactions that achieve developmental consistency. Neural crest
cells reveal how such systems can change and evolve. They are modified by the tissues
through which they migrate, and in turn induce changes in some of those tissues.
Some of the effects are physical, some chemical, and some involve gene regulation. A
most satisfactory discussion is provided by Eva Jablonka and Marion Lamb in
Epigenetic Inheritance and Evolution (1995), where the emphasis is on non-DNA systems,
transcellular inheritance, and the possibility of transgenerational inheritance.
Non-DNA Epigenetic Inheritance Systems

As outlined above, the cytoplasmic inheritance of permease can give rise to two
biochemical lineages in E. coli. Jablonka and Lamb provide a model that suggests how
this could have been established by an ephemeral environmental stimulus. This has a
general theoretical relevance for the kinds of internalization of environmental stimuli
that fascinated Ivan Schmalhausen and C. H. Waddington.
Cytotaxis is the inheritance of induced changes in the cortical architecture of
unicellular ciliates, without reference to their nuclear DNA. Its existence has been
known for the last 30 years. Also known as directed assembly, it has since been
found in mammalian cells in culture, and in the epidermal cells of caterpillars.62 That
the cytoplasmic architecture and non-genetic chemical make up of the ova of multi-
cellular organism is responsible for a number of the earlier stages of epigenesis has also
been accepted for a long time.
Chromatin marks are defined by Jablonka and Lamb as the non-DNA parts of the
chromosomes, for example binding proteins or additional chemical groups attached
to DNA bases that affect the nature and stability of gene expression.63 Chromosomes
in different cell lineages have different chromatin marks, which may change during
the course of development, reflecting the activation status of the genes concerned. The
chromatin marks that characterize particular developmental lineages of differentiating
cells are largely passed on to the daughter cells. When DNA is being replicated, the
methylation of the parent strand remains, but initially the daughter strand is not
methylated until methyl transferase responds to the asymmetry by methylating the
appropriate cytosine bases of the new strand. Similarly, the new strand lacks histones,
and these are synthesized and assembled under the direction of protein transferase.
Some errors in methylation are random, others seem to be directed by a modifier
molecule or an environmental stimulus that acts through one. Almost as stable as
point mutations of DNA, they are much more frequent. Jablonka and Lamb argue that
chromatin mark systems are a key to understanding epigenetic evolution:
Since the chromosome-marking maintenance mechanisms are independent of the functional

state of the gene, and the gene product is not required to have a specific regulatory role, the
system is potentially much more flexible. It is able to change both during development and
during evolution.64
They point out that the genotype, including modifier genes and their products that
participate in epigenesis, is relatively constant, but the non-DNA components of
epigenesis exist in numbers and variations that provide for an almost unlimited com-
binatorial creativity. In addition, an acquired change to the non-DNA epiphenotype is
more easily inherited than one that requires incorporation into the DNA itself. Several
clear examples of such inheritance persisting through meiosis are known in protozoa.
Beneficial qualities are more likely to persist, and, if heritable, likely to strengthen
homeorhesis.
Methylation
For transcription to messenger RNA, DNA must be chemically as well as physically
available. Its cytosine bases must be free of methylation, which is common in
inactive DNA, and takes it out of the running for transcription even when it is
uncondensed. Methylation involves the post-synthetic addition of methyl groups to
cytosine bases, often found in CpG dinucleotides and associated with promoter
252 Chapter 6
regions. It changes the fit between the major groove of the DNA double helix and
DNA-binding proteins. Methylation of histone tails also changes the interplay
between acetylation and methylation of histones that affects chromatin structure.
Specific types of proteins are capable of recognizing acetylated histones or methylated
DNA, such as the methyl-CpG-binding proteins (MeCPs or MBDs). Whole complexes
of chromatin remodeling factors are known to restructure local chromatin architec-
ture, capable of converting areas between transcriptionally open or closed
conformations. Methylation, which is caused by the enzyme methyl transferase, is not
random, but a regulated procedure that ensures that differentiating lineages of
embryonic cells only produce the proteins appropriate to their special requirements.
Since methylation is absent from yeast and rare in Drosophila, there must be other
ways of silencing DNA.
Imprinting
Mendelian genetics assumed that a gene is a gene, and the action of a gene in an
organism was not affected by the sex of the parent who contributed it. But the
phenomenon of imprinting has such implications. Two apparently different genetic
diseases of humans are caused by the same mutation, but the phenotypic expression
of the gene as one or the other of the two conditions depends on whether it came
from the mother or the father. The sex of the parent somehow has an imprinting effect
of the offspring. Moreover, whatever parent the imprint comes from in the previous
generation, the imprinting is re-set according to the sex of the individual who will be
a parent of the next one.
The case for methylation as one of the causes of imprinting is promoted by Marilyn
Monks 1995 essay Epigenetic programming of differential gene expression in
development and evolution. Methylation patterns that may have developed onto-
genically in a parent are undone during gametogenesis, but the ovum is slightly
methylated, and the sperm slightly more so, to allow imprinting by each parent. The
methylation mechanism regulates the expression of the gene, but is not itself coded
in the DNA. The mechanism falls outside the genic paradigm, but has to be
encompassed by the epigenetic paradigm.65
In Monks mice, the degree of methylation is at its lowest overall in the blastocyst
stage of development, perhaps because the methyl transferase laid down in the
cytoplasm of the egg by the mother has been gradually degraded and diluted by cell
proliferation, and the embryo has not yet begun to synthesize its own enzyme. The
germ line cells continue to be minimally methylated, but extra-embryonic tissues are
progressively methylated, and the rise is even steeper in the somatic cell lineages.
Methylation patterns of the latter are responsible in part for their differential features.
Although there are a number of hypotheses regarding the value of imprinting in
relation to organismic integrity, such as avoiding competition between the mother
and the implanted embryo, Monk wonders if imprinting per se is simply a carry-over
of methylation that had been primarily correlated with gametogenesis. More recent
work has suggested the presence of cytoplasmic factors in the oocyte in addition to
DNA methyl transferase (DNMT) can perpetuate imprints, including heterochromatin
protein 1 (HP1) which recognizes methylated histones, and other transcriptional
repressors. In mammals, imprinted genes are clustered into differentially methylated
regions (DMRs), and this may protect imprints from the global methylations and
demethylations that occur in embryos. Mammalian cloning, which made Dolly the
sheep an international media star, involves the technique of somatic cell nuclear
transfer. The nucleus of a differentiated cell is transplanted into the rich environment
of an oocyte which has been stripped of its own genetic complement. This shows how
epigenetic patterns can be reversed, since differentiated nuclei can revert to
totipotency and (albeit rarely) provide for the whole of development. The failure of
most cloning attempts of this type proves how important epigenetic patterns are, and
that a complete DNA sequence complement is not sufficient to direct the cell cycle.66
How might these waves of demethylation and remethylation have evolved? Some
argue that they provide the advantage of erasing any potentially damaging epigenetic
modifications incurred in the parent. The existence of methyl groups on cytosine
bases greatly increases the risk of a point mutation, in that these 5-methyl-cytosines
are often spontaneously deaminated to thymine bases. Another correlation could be
the relative activity of transposable elements, known to be more highly expressed in
germ linepossibly as a result of the global demethylation. However, there is growing
evidence for the persistence of methylation and histone-binding patterns between
generations that amount to a neo-Lamarckist process of the inheritance of acquired
characteristics. This will be discussed below.
Found in a variety of animals, methylation reaches its most extreme form in some
insects, where the entire chromosomal complement derived from a particular parent
might be silenced as heterochromatin, or lost entirely. Removal of the previous
generations methylation patterns in the early embryo is conventionally interpreted as
the result of strong selection against carrying the remnants of an individuals
epigenetic history into the next generation.67 This is not a barrier to any emergent
novelty of epigenesis that is based on DNA point mutation, exon shuffling and trans-
posable element effects in the parental germ line. But Jablonka and Lamb wonder if
there is any exceptional transgenerational inheritance of adaptive chromatin marking,
particularly methylation patterns. In the fruit fly, methylation of transgenes, i.e.,
foreign genes experimentally transplanted into host cells, persists from one generation
to the next. Persistent methylation of transgenes also occurs in protists, plants, fungi,
flatworms, nematodes, crustaceans, insects, and mammals, including humans. Plants
offer the bulk of the examples, and this is because somatic cells that may have been
exposed to environmentally induced epigenetic changes enter the germ line quite late
254 Chapter 6
in the plants development. Barbara McClintock found that inactivation of the

jumping genes of corn during epigenesis was heritable; methylation is responsible.
Examples of heritable chromatin mark alterations are relatively sparse. Since
methylation of the cytosines of nucleic acids is a relatively recent discovery there was
no early guiding hypothesis for phenomena that did not obey Mendelian rules, except
some kind of aberrant change in DNA. Chromatin mark changes may be random, as
well as directed by environmental change. Early neo-Lamarckists were fascinated by
highly visible somatic phenotypic responses to environment, but did not have exper-
imental or observational access to changes that might occur in the germ line in early
embryogenesis. Looking in the right places with modern molecular techniques and a
working hypothesis based on methylation effects is now expanding the body of
evidence pertaining to non-DNA inheritance systems. Leslie Pray (2004) reviews some
current research on the inheritance of methylation patterns, and histone binding,
under the title Epigenetics: genome, meet your environment, commenting that as
the evidence accumulates for epigenetics, researchers reacquire a taste for
Lamarckism.68 This article shows how the mainstream comes closer now to the
Jablonka and Lamb direction.69 These are indeed heritable changes, but strictly
speaking, they are neo-Lamarckist effects, and some are detrimental conditions
produced under stress.
Epigenetic Effects of Environmental Stress

Compounding methodological problems is the scarcity of information on what envi-
ronmental changes affect chromatin structure in such a way as to alter gene
expression, and activate enzymes, repair mechanisms, and changes in transposon
action. The role of heat-stress proteins in response to physicochemical stresses has
already been discussed. Recombination is increased by the effect of heat stress on
highly condensed chromosome regions. The same stimulus increases the vulnerability
of DNA to the action of transposable elements, whose activity is also modified by
changes in their chromatin structure. Such examples show that the environment can
have an efficient causal effect.
The potential of a genome to respond to stress was called catastrophe insurance
by Koch (1993). (Recollect that I have defined stress as a condition that requires
abnormal and energy-demanding compensatory responses.) But the genome responds
in a larger context of behavior, physiology, and environment. For example, stress
arises from the domestication of wild stock, where behavior is restricted and new envi-
ronmental regimes are imposed. Hormonal effects on domestically bred silver foxes,
and the parallel case of Djungarian hamsters, have already been mentioned. Another
example is the Laysan duck, whose entire population arose from a low of ten
individuals 90 years ago. A few birds that were subsequently domesticated began to
produce novel plumage colors within a few generations. Since the ducks had already
been inbred for most of their history, alteration of the color of the feathers is less likely
to have arisen from continued inbreeding than from the domestic breeding
environment.70 A natural parallel may be the rapid speciation that occurs in isolated
and limited environments such as islands, and in new lakes, as a result of stressful
changes in behavior and social structure, as well as physicochemical differences. As
ever, note that the typical agents of natural selection, competition and predation, are
absent under those circumstances.
Stress responses can come from molecular mechanisms other than heat stress
proteins.71 Mutability is known to increase in bacteria under stress, which in a natural
setting may be most of the time. Moreover, some eukaryotes that normally reproduce
asexually switch to sexual reproduction, thus increasing variability through recombi-
nation. In a range of effects of environmental change, the least stressful simply alters
gene expression through slight alterations in chromatin marks. If the lineage has
experienced periodic, specific stress, such as the lack of an essential nutrient, pre-
existent mechanisms may be activated. One example is directed or adaptive
mutagenesis in bacteria. General stress, such as change in oxygen tension or
temperature change, may increase gene duplication and mutation, resulting in
increased physiological adaptability. Acute stress may result in the activation of error-
prone DNA repair mechanisms, increase in the activity of transposable elements, and
crossing over during meiosis.
Catastrophic Stress
If stress has such a prominent epigenetic impact, the expression catastrophe
insurance is doubly significant. Canalization might be loosened as a direct result of
catastrophic environmental change. I have noted that major emergent forms often
arose before major bolide or geophysical disasters, and then diversified explosively in
their wake. Catastrophes cleared the bench of the usual agents of natural selection,
allowing earlier natural experiments, especially those with emergent adaptability, to
multiply and diverge. But this does not exclude the possibility that some new
emergences might have occurred as a direct result of sublethal heat shocks occurring
at the fringes of impact or volcanic blast zones. Because water buffers heat, slow
sustained rise in temperature would be more likely for aquatic organisms than sudden
heat shock. But that might be even more effective than a transient stimulus.
Canalization in hopeful emergents might have been loosened as a direct effect,
thereby stimulating rapid diversification. In addition, small, highly stressed
populations of survivors would have been involved. The combination of an imposed
founder effect with physical and biological environmental changes, especially altered
interactions between individuals, would have had some effect on epigenetic
variability.
256 Chapter 6
Origin of Epigenetic Inheritance Systems
Epigenetic inheritance systems are of major importance in multicellular organisms

where true-to-type lineages must originate and reach their predictable goals as parts of
complex mature forms. But how and where did the epigenetic inheritance systems
originate? John Bonner (1974) calculates that the multicellular condition has emerged
independently at least seventeen times, the major products being plants, fungi, and
animals. (All animals are presently considered to have arisen from a common,
probably unicellular, ancestor.72) Simple multicellular organisms had the emergent
qualities of being hard to eat and slow to starve. Without much differentiation, they
also had an easily realizable potential to eat larger things, store more food, locomote
more efficiently, and commit themselves more effectively to reproduction. Looking at
the progressive evolution of ever higher emergent levels, Bonner (1988) saw that while
there is no strong correlation between genome size and phylogenetic status, adaptabil-
ity and the number of different cell types are correlated. Higher plants have about 30,
higher invertebrates have about 55, vertebrates more than 120.
It could be argued that epigenetic inheritance systems participate in the cell cycles
of unicells, and are not therefore novel emergent qualities of multicells. Yet there is
novelty in the emergent qualities of chromosome packaging and methylation
mechanisms. And it is in multicellular organisms that differentiation is so dramatically
complexifying. As Erasmus Darwin and Herbert Spencer speculated long ago, the dif-
ferential effect of the physicochemical environment on a multicellular eukaryote
would alone be sufficient to prime cellular differentiation in every generation, without
DNA-epigenetic inheritance systems. These effects are seen in some quasi-colonial
unicells, provided that the appropriate environmental stimuli are constantly present.
DNA-epigenetic systems are necessary for the complexity of multicellular organisms,
but they may all have arisen through interaction with environmental effects. And they
also require complementary factors such as adhesion/integrin molecules, cell
junctions, and the establishment of intercellular induction mechanisms.
The elaboration of skeletal matrices that would physically affect tissue assembly
would also enhance structural organismic integrity. Cellular cytoskeletons, integrins,
the basement membranes of epithelia, and cell walls, as well as the more visible
structures found in sponge skeletons, coral concretions, mollusk shells, chitinous
exoskeletons, echinoderm spines and plates, and vertebrate cartilages and bones all
contribute to the self-assembly of tissues and organs.
Jablonka and Lamb note that epigenetic inheritance systems had a double role in
the transition to complex multicellular organisms:
First, they enabled the emergence of a new unit of structure and function, the phenotypically
distinct cell lineage. Second, they allowed the formation of the stable interdependences between
epigenetically distinct cell lineages, which resulted in the evolution of integrated organism from
loose groups of cells.73
They also anticipated Newman and Mller (2000) with their argument that the
phenotypic epigenetic changes produced by extrinsic and intrinsic environmental
effects were prior to their canalization by genetic assimilation and natural selection.
Sexual Reproduction
Bell (1988a) asserts that the absence of sexual reproduction kept living organisms in a
primitive unicellular state for about 2 billion years. Furthermore, natural experiments
in multicellularity may often have been tried during that time, but failed because of
the lack of the repair facilities that emerged with meiosis. Thus, the tradeoff between
faithful reproduction and experimental flexibility held early progressive evolution
back until a saltatory boost arrived in the form of sex. For most of the time in question
prokaryotic unicells could complexify themselves by gene acquisition through a
variety of routes, and could reproduce asexually. Although some engaged in
conjugation, which falls within a loose definition of sexual mating, sex in eukaryotes
involves chromosomes. Chromosome packaging was an immediately advantageous
feature for mitotic asexual reproduction, and it potentiated sexual reproduction as
well. Membrane adhesion molecules, and the pre-existent experience of conjugation
were other generative features. The natural experiment of sexual reproduction
succeeded because of the prior lack of reconditioning mechanismsthere was nothing to
prevent it at that stage. Once in place, repair mechanisms could be refined, and a new,
efficient level of change-resistant dynamic stability (i.e. homeorhesis) established.
In sexually reproducing organisms it is common for there to be impregnation of a
haploid egg by a haploid sperm, returning the number of chromosomes to the diploid
or double number characteristic of the type. This is sexual reproduction, but did not
initially require the differentiation of sex chromosomes and phenotypically distinct
(dimorphic) genders. Those emerged later and independently in different plant and
animal lineages. The familiar Y chromosome of human males probably appeared early
in the mammalian lineage. It retains sufficient of the collinear genes of the X
chromosome to demonstrate that it arose from such an ancestor. The major sex-
determining trigger is the protein synthesized by the SRY gene (sex-determining
region Y), although there remain a number of housekeeping genes that operate in
every cell. Once maleness has been catalyzed, a number of genes from other
chromosomes are involved in the final determination of gender in the mature
mammal. Testosterone production in the testes is an important part of this process.
The Y chromosome retains the ability to pair with the X chromosome at synapsis
during Meiosis I of gametogenesis, but for most of its length it is incapable of crossing
over with the X chromosome. As Karin Jegalian and Bruce Lahn (2001) write in Why
258 Chapter 6
the Y is so weird, the Y chromosome retains much of its evolutionary history because
of the lack of recombination:
. . . the Y lost the ability to swap DNA with the X in an unexpected, stepwise fashionfirst
involving a swath of DNA surrounding the SRY gene and then spreading, in several discrete
blocks, down almost the full length of the chromosome. Only the Y deteriorated in response to
the loss of X-Y recombination, however; the X continued to undergo recombination when two
copies met during meiosis in females.74
Now, I have already inferred that a number of molecular processes from DNA
mutations, jumping genes, and chromosomal mutations are all-or-none saltations. As
these authors express it we here have an example of saltation through chromosomal
mutation when the first chunk of the proto-Y containing the SRY gene inverted. The
leap at that stage was neither advantageous nor detrimental; but it might have resulted
in reproductive isolation of the organisms in which it happened. This was around the
time when the mammalian lineage separated from the reptiles. Further inversions
seem to have occurred at or close to the bifurcations of the mammalian line that gave
rise to the placentals, and anthropoid primates (monkeys, apes and humans). Use-it-
or-lose-it is invoked to explain the deterioration and shrinkage of much of the Y
chromosome.
The emergence of chromosomally different sexes was accompanied by sexual
dimorphism This has evolutionary implications since the fate of future generations
now depends on the reliable interaction of two sets of gametes in two organisms that
have not only developed as differentiated genders, but may not only look different as
mature organisms, but in the case of animals may behave differently, use different
resources, and thereby complexify their ecological niches. Furthermore, the necessity
of sexual interaction is what potentiated the familial interactions of the higher
mammals.
Summary of Epigenetic Mechanisms
1. Point mutations of the genes that code for structural proteins and enzymes have a
role in adaptational and adaptability evolution. More important for epigenetics are
numerous genes that can modify structural gene activity by coding for regulatory
proteins and enzymes, or by interacting with the regulatory proteins to act as switches.
Alteration of these controlling mechanisms may contribute to epigenetic evolution.
2. In the egg and the early embryo there are gradients of regulatory RNA and protein
molecules whose alteration may affect thresholds of activity and have an evolutionary
effect, prior to involvement of the genome of the new organism.
3. Modifier genes and the actions of their products are hierarchically controlled, so
that a single alteration can have a multiplier or cascade effect.
4. The action of transposable elements, in amplifying or changing established

regulatory patterns, can be a mechanism for radical epigenetic change. In many cases
this is a non-random process. While epigenetically potent, jumping genes lack the
risks of point mutation.
5. Non-DNA influences such as chromatin marks, involving methylation and histone

binding, can be initiated by environmental stimuli. These can in some limited
instances be inherited.
6. Consistent reduplication of genes to produce gene families and repetitive differen-

tiation is assured by the action of transposable elements and by mutations involving
recombination enzymes.
7. Genetic drives, involving codon amplification, gene duplication, concerted

evolution, and variant repeats (repetitive differentiation), may be responsible for
allometric growth during development and for the phenotypic phenomenon of ortho-
genesis.
8. Concerted evolution ensures that all of the members of a clade possess the same
pattern of repetitive differentiations.
9. Novelty in structural genes is not only caused by point mutation, but also by new
cistron combinations, intragenic duplication, exon shuffling, and the conversion of
introns to exons. Mutability is increased through methylation and the weakening of
repair mechanisms under stress.
10. There are deep homologies among selector genes, e.g. Hox and Pax, that contribute
to atavisms, saltatory changes, and parallel and convergent evolution.
11. The role of retroviruses in transphyletic exchange of genes is real and known in a
few cases to be advantageous, but its general significance is enigmatic.
12. Genes participate in epigenesis, and genes are regulated by other genes. These
activities are, however, controlled by non-genetic factors. Within the organism, these
include chemical heterogeneity and changes in the ultrastructure of the cytoplasm,
the shape and size of cells and epithelia, and the proximity of chemical and physical
inducers in the internal milieu, and the behavior of organizer cells. Development and
260 Chapter 6
epigenetic evolution are expressions of the whole organism and its female parent
operating in the larger environment, as well as expressions of genes.
13. Some epigenetic inheritance systems, such as cytoplasmic composition and archi-
tecture of the egg are not coded in DNA but can alter the phenotype of the offspring.
Within a given species the size of the egg alone can be enough to drastically alter the
form of the developing embryo. Non-DNA maternal effects can carry the embryo
through its early stages and influence the establishment of its cell lineages before its
own gene-based, epigenetic organizing mechanisms kick in. Moreover, maternal
effects that are altered by prolonged environmental change may ultimately be
genetically accommodated.
14. The semi-independence of embryonic cell lineages, and their internal hierarchical
arrangement makes it possible for radical epigenetic change to be integrally accommo-
dated in emergent organisms. It also allows the orderly shutdown of multiple cell
lineages during paedomorphosis.
15. Subsequent to emergent epigenetic changes, the fine tuning of homeorhesis

becomes a general quality of a clade (or of the cell lineage). The more dynamically
stable (or generatively entrenched) these systems are, the tighter canalization
becomes. Development is more likely to keep true to type.
16. Intron dissemination, repetitive differentiation, molecular drive, self assembly,

anticipation, and other aspects of complexification can occur without causal reference
to adaptivenessin other words, out of the sight of natural selection.
17. The greatest challenge for developmental evolutionary theory is the difficulty of
modeling epigenetic programs that would contain all of the real variables that have
affected evolution.
Afterwords
The Dover TRAM

Although I compiled the above material independently, from a variety of sources,
Gabriel Dovers book Dear Mr. Darwin (2000) brings together similar mechanisms with
evolutionary potential under the heading of TRAM systems, an acronym for
Turnover, Redundancy, and Modularity.75 Although I agree with the comprehensive
principles that Dover is trying to establish I will not borrow his acronym. Turnover
could apply to mitosis, meiosis, recombination, gene transposition, and gene
conversion, all of which could undergo evolutionary experiment through unequal

crossing over, DNA slippage and molecular drive. So it is difficult to remember all of
its implications. Redundancy is redundant, since it is a subset of modularity.
Nevertheless, Dover makes the important point that co-evolution of compensatory
molecular systems could allow sublethal experimental results to persist. At the
molecular level, modularity applies to codons, exons, genes, protein domains. Such
modules, or holons, make it possible to produce new genes and proteins, both
regulatory and structural. Then, there are cellular modules involved in development
and hence in epigenetic evolution. The interaction of modules is a necessary aspect of
self-organization. It is therefore essential to remember that the organism is greater
than the sum of its modules, regardless of the level at which analysis is focused.
Beyond that, do not trams run in directions determined by their environment (in the
form of rails?).
Environmental Direction
Environmentally induced epigenetic inheritance system changes, usually involving
methylation patterns, are common in unicells and plants, where the germ lines are
not isolated from early development. The evidence from animals is sparse, perhaps
because animal epigeneticists have not thought to look for it. Even if animals have not
been generally influenced by these kinds of epigenetic effects, there would still be an
important distinction between plant and animal evolution that needs elaboration.
Genetic assimilation, or the larger category genetic accommodation falls between
non-DNA epigenetic inheritance and conventional natural selection of alleles, but the
process could just as well be called environmental direction. Unquestionably the
environment can induce phenotypic change that involves ontogenic modification of
existing heritable genetic factors. Their adaptiveness is also altered before any
change in the genes themselves. Where there is a coincidental competitive advantage
arising from these phenotypic modifications, any directional genetic shift will
reinforce anatomical change. Internally, as Schmalhausen proposed, coordinative
conditions that are energetically economic, and autonomization of environmental
stimuli will lead to greater stability, and tighter canalization. And as Newman and
Mller say, gene change is after the fact of epigenetic change.
Natural Genetic Engineering

Before Darwin voiced any thoughts on the matter, the English evolutionist W. C. Wells
commented that what breeders do by art seems to be done with equal efficiency,
though more slowly by nature.76 At the conclusion of my book Evolutionary Theory:
The Unfinished Synthesis (1985) I paraphrased this to ask Is what genetic engineers do
by science done with equal efficiency, though more slowly by nature? James Shapiro
had already anticipated that question in 1977, with the multifold actions of transpos-
262 Chapter 6
able elements in mind. The tools of genetic engineersplasmids and various enzymes
for snipping and splicingare all borrowed from nature. And transgenes are natural
structures slipped into a foreign genome, an operation not all that different from
natural bacterial transformation and retroviral transgenesis. Shapiro extends the simile
in his 1992 essay Natural genetic engineering in evolution:
. . . evolutionary novelty often does not reside in the invention of new biochemical processes by
the continual modification and selection of individual proteins. Instead evolution appears to
proceed by the utilization of basic biochemical routines in different combinations in different
organisms. With few exceptions, the structural proteins of all mammals, for example, are
probably interchangeable; what makes a mouse different from an elephant is when and how
those molecules are synthesized and assembled during development. . . . Much of genome
change in evolution results from a genetic engineering process utilizing the biochemical systems
for mobilizing and reorganizing DNA structures present in living cells.77
From the large catalogue of information about the causes and effects of molecular
modification, all that the proponents of the Modern Synthesis have chosen to explain
evolution is the accumulation of adaptive random mutations by an infallible
metaphorical force. This is not only hopelessly narrow, but scarcely even relevant to
Shapiros radical way of thinking. He properly demands that any known mechanisms
that can bring about change through an orderly hierarchical rearrangement of gene
expression must be integrated into evolutionary theory. He points to some cases of
large-scale genomic change, such as the chromosomal fragmentation and reintegra-
tion that occurs in ciliates during reproduction. The cascade of DNA effects that result
in the enormous array of antibodies in vertebrates belong in this category too. I have
already described the changes caused by transpositions that lead to hybrid dysgenesis
in some Drosophila. Some of the offspring of any animal that had multiple ova and
sperm altered by transposable elements, would be ready to form a distinct new lineage.
We know that genomic and organismic integrity is retained in such cases, so we are
further along in answering Batesons perennial question about the accommodatory
mechanism.
J. H. Campbell, who is quoted at the heading of this chapter, takes the view that
mechanisms of genome regulation have evolved to meet the goal of providing
novelties of variation rather than for ensuring the continuance of the status quo. Some
jumping genes could certainly fit the role of active agents of potential evolutionary
change. Others are provided by Lynn Caporale (2003). To continue the engineering
metaphor, epigenetic mechanisms provide a variety of machine tools, which do not
produce particular products, but make the specialized tools that do. However, the
inference that epigenesis is genetic in the narrow sense of being all to do with genes
and their expression comes from the genocentric universe, where other factors are
completely ignored. The major achievement of Jablonka and Lambs Epigenetic
Inheritance and Evolution (1995), nicely dedicated to parents who gave us more than
genes, is to move us toward a system centered on organismal holism, which in turn

wheels around in the larger environmental sphere. This is complemented by Susan
Oyamas philosophical propositions concerning epigenetic evolution (Oyama 1985
and 2000).
Epigenetic Algorithms
Mechanical metaphors have appealed to many philosophers who sought materialist
explanations of life. The definitive work on this subject is T. S. Halls Ideas of Life and
Matter (1969). Descartes, though a dualist, thought of animal bodies as automata that
obeyed mechanical rules. Julien de la Mettrie applied stricter mechanistic principles to
humans in LHomme machine (1748). Clockwork and heat engine models were popular
during the Industrial Revolution. Lamarck proposed hydraulic processes as causes of
variation. In the late nineteenth century, the embryologists Wilhelm His and Wilhelm
Roux theorized about developmental mechanics. However, as biochemical and then
molecular biological information expanded, popular machine models were refuted,
but it is not surprising that computers should have filled the gap. Algorithms that sys-
tematically provide instructions for a progressive sequence of events seem to be
suitable analogues for epigenetic procedures.
A common error in applying this analogy is the belief that the genetic code, or at
least the total complement of an organisms DNA contains the program for its own dif-
ferential expression. In the computer age it is easy to fall into that metaphysical trap.
However, in the computer age we should also know that algorithms are the creations
of programmers. As Charles Babbage (1838) and Robert Chambers (1844) tried to tell
us, the analogy is more relevant to creationism than evolutionism. At the risk of
offending the sophisticates who have indulged me so far, I want to state the problems
in the most simple terms. To me, that is a major goal of theoretical biology, rather than
the conversion of life to mathematics.
DNA contains information that can be transcribed into RNA sequences, and then
translated into proteins. It also contains promoter sequences that constitute on and
off switches for transcription. Some of the RNA and proteins that are synthesized can
flip those switches; and some of the regulator molecules are the products of enzymatic
reactions. So the big question is, where is the program of instruction, or epigenetic
algorithm, that can tell those mechanisms where and when to operate? Although
promoters in bacteria are quite well understood, the number of binding sites on the
promoters of eukaryotic chromosomes are considerable. If combinations of bound
sites are involved in downstream gene regulation the potential number of activations
is astronomical. For example, there is a multifunctional protein involved in sea urchin
development whose primary sequence is coded by a structural gene endo16. Its
promoter sequence is known to have 50 binding sites, for 20 of which there is a known
binding factor.78 This promoter molecule, and hypothetically all other modifying
264 Chapter 6
molecules, might be thought to contain an algorithm that demands precise outputs in

response to molecular inputs, though it would be stretching the point to describe the
system as a computer. Nor is it an algorithm for development. It is an algorithmic
switching mechanism for the regulation of endo16 protein production. Presumably
many structural genes are regulated in similar ways, making for a highly complex array
of switches waiting to be differentially activated by proteins and steroids during
development. The cells of the developing organism can also be considered to be
algorithmic, since they mediate between regulatory messengers coming from other
cells in the embryonic milieu. If there is such a thing as a biological computer it is the
whole organism, which also happens to be the computer operator and service
technician.
Hypothetically, in a simple unicell, all systems could go all out until the cell reaches
critical mass and then divides. But this ignores all kinds of problems about acquiring
nutrients, making choices of biochemical pathways, and generally maintaining
cellular homeostasis, especially in a changing environment. Without there being any
change in the DNA or RNA of that unicell, physiological strains can diverge and
persist.
In a multicellular organism, the first few cell divisions may occur through simple
mitosis, without any differential expression of nuclear DNA. But the cells can differ-
entiate as a result of the heterogeneity of the fertilized egg, such as is provided by the
distribution gradient of the messenger RNA that codes for bicoid protein in
Drosophila.79 The concentration of the protein is an epigenetic factor in the sequential
differentiation of the anterior series of embryonic structures. The heterogeneity of the
egg usually constitutes a heritable pattern, but is it constructed by a genetic program,
or by the totality of the female organism? In this case, probably the former, but there
are other cases in which the females nutritional condition, and therefore her behavior
in the face of ecological encounters, are certainly influential. Matsuda (1987) demon-
strated how the amount of yolk laid down in crustacean eggs would affect
development.
In early epigenesis, DNA regulation soon becomes involved in cellular divergences,
and the activating mechanisms are often the end products of protein synthesis and
their enzymatic actions. But often those are affected by the physicochemical condition
of the developing organism, and from the larger environmental conditions that lie
beyond. Epigenesis does not start with the genes nor finish with the genes. Nor does
it start and end with the environment nor any hierarchical level between it and the
gene. But the system could not work without the participation of all those levels
which is essentially the interactionism of Susan Oyama (1985). Pinning down bits
of epigenetic algorithms at the gene level is possible, but understanding the operation
of the whole organism is not made much easier by seeing it as a computer.
Is It Lamarckism?
Lamarck applied four laws to progressive and adaptational evolution. The two that
refer to a trend to increase in overall size, and allometric growth in proportion to
utility can be understood in broad epigenetic terms. Another states that the organism
responds to needs. Logically, the metaphor is equivalent to the idea that the
organism responds to selection pressures. But there is a deeper reality to Lamarcks
version: Any organism has the real and essential feature of responsiveness. If it is an
animal, it also has greater freedom to behave in a variety of ways. And if it keeps
behaving in the same way it may be constantly subjected to the same environmental
influences. As I have emphasized in previous chapters, this will result in some
ontogenic, phenotypic changes that might eventually be genetically accommodated.
The speed at which the genotype co-opts the phenotype will depend on how varied
and numerous the genetic molecular experiments are, and how lucky the correspon-
dence between them and the current actions of the organism are. But in the meantime
the animal is not restrained from continuing to behave in a particular way, nor from
changing its habits. The more adaptable it is the more freedom it has, although it risks
regression if it specializes too much.
Unlike the neo-Lamarckists, Lamarck did not believe that multicellular organisms
acquired characteristics imposed directly by the environment. But in its essentials
Lamarckism involved an autonomous evolutionary progress modified by response to
the environment. For him, the inheritance of acquired characteristics was not the
crucial law, and he believed it could get in the way of gradation to more complex
forms. As Richard Burkhardt Jr. convincingly argued in The Spirit of System (1977),
modern biologists and philosophers have lost sight of what mattered to Lamarck, and
taken the inheritance of acquired characteristics to characterize his thought. Suppose
we were to continue to insist that the crux of Lamarckism comes down to the
inheritance of acquired characteristics; to what extent might it be possible?
Early in this chapter I gave an example of a cytoplasmic feature, the presence of
permease in bacteria, that is passed on to future generations, and so establishes
distinct physiological strains, without DNA involvement. This is literally the
inheritance of acquired characteristics, and would probably have satisfied Lamarck.
Transgenerational methylation patterns and other chromatin marks are in the same
category.
The acquisition of foreign genes, or paraheredity, can occur in bacteria through
transduction and conjugation. The emergence of the endosymbiotic eukaryote was a
major feat of whole genome acquisition. Eukaryotes can also pick up exotic genes
through the action of parasitic bacteria like Agrobacterium tumefasciens and retro-
viruses. The genome projects are shedding some light on this, and such effects are
more common than previously thought. But the acquisition of heritable characteris-
tics is not the inheritance of acquired characteristics.
266 Chapter 6
Lamarck understood that adaptation, however it came about, could get in the way
of evolutionary progress. In contrast, Darwin, who finally imported the inheritance of
acquired characteristics into his own theory, thought that adaptation through natural
selection was the mechanism of evolution. And the ultra-Darwinists have taken that
interpretation to extremes. When Lamarck inferred that the organism could respond
to environmental change he was right, in the sense that if the organism was already
adaptable it could make the appropriate changes in its behavior and might finally
acquire appropriate anatomical modifications.
What about neo-Lamarckism, a synthesis even more elastic than neo-Darwinism?
There are two specifics that neo-Lamarckism added to Lamarckism: the environment
can directly cause changes in the organism; the changes are heritable and, though
random, some are advantageous. Therefore it is within neo-Lamarckism rather than
Lamarckism that heritable changes in methylation and histone binding patterns
should be placed.
Neo-Lamarckists also adopted physiological and behavioral adaptability.
Physiogenic change imposed by the environment has been an important part of phys-
iological evolutionary history, and some environmental stimuli, such as heat shocks,
can loosen canalization and increase transposon activity with heritable consequences.
However, if these are changed by the environment, they should be interpreted as neo-
Lamarckist rather than Lamarckist.
Lamarck properly emphasized the importance of choices made by individual
organisms for subsequent evolution, something that was lost by the population
thinking of the Modern Synthesis. In animals especially, specific behavioral responses
to environmental changes are important, and the higher the emergent level of
physiology and behavior the more choice the animal has. Neo-Lamarckists properly
emphasized the effect of the environment on the individual, with the qualification
that it was not always beneficial. Beneficial or not, there seem to have been many
incidents of emergent evolution that either would not have occurred or would not
have succeeded, without disequilibration of internal or external environment. I dont
accept the inheritance of acquired characteristics, in the sense of environmentally
directed adaptive gene construction, but I do appreciate that Lamarck was closer to a
generative theory of evolution than Darwin.
7
Orthogenesis
In many other cases, modifications are probably the direct result of the laws of variation or of
growth, independently of any good having been thus gained. But even such structures have
often, as we may feel assured, been subsequently taken advantage of, and still further modified,
for the good of species under new conditions of life.
Charles Darwin, 18721
Organisms develop in definite directions without the least regard for utility, through purely phys-
iological causes, as the result of organic growth.
Theodor Eimer, 18982
Darwin wrote that laws of growth were independent of natural selection, giving the
example of ubiquitous hooks on the stems of bamboos, which gave no advantage to
normal plants, but which were turned to good use by creeping and climbing bamboos.
As his epigraph implies, he believed that trends of variation could be emerge without
initial selective value, though the affected lineage might find them advantageous at
some stage. St. George Jackson Mivart (1871) had argued that innate tendencies of
growth were responsible for the parallel evolution in tooth structure between
marsupials and placental mammals, although the parallel features had been absent
from their common ancestors.
The quotation from Eimer gives some of the sense of the law of growth named
orthogenesisit implies an evolutionary process that goes in a definite direction
through an autonomous drive. Many examples of directional exaggerations of
particular anatomical characters, which come under the category of allometry, are to
be found in the fossil record. Enlargement of the canine teeth in evolutionary lines of
saber-toothed cats, and the increasing proportions of the antlers of the Irish elk are
well known. Since those lines are extinct, orthogenesis was thought capable of uncon-
trolled ultramorphosis to a form that could not easily survive. Although orthogenesis
cries out for re-invention, and belongs with developmental evolution, I have saved
this discussion until its molecular context could be set out in the previous chapter on
epigenetics.
268 Chapter 7
Once a respectable evolutionary idea, orthogenesis was prominent in textbooks

until the 1940s. The particular concept of straight-line and definitely directed
evolution was introduced by Wilhelm Waagen in 1867. Wilhelm Haake, who coined
the word orthogenesis, and Theodor Eimer, who popularized the concept, regarded
it as the effect of an autonomous force or drive.3
Some modern evolutionists believe that developmental constraints might be
responsible for phyletic trends, something Richard Goldschmidt had considered in
1940. They ignore his further proposal:
What is called in a general way the mechanics of development will decide the direction of
possible evolutionary changes. In many cases there will be only one direction. This is orthogen-
esis without Lamarckism, without mysticism.4
At one time it was proposed that human evolution had an orthogenetic component.
The Australopithecus and Homo series both show progressive phenotypic paedomor-
phosis. Bolk (1926), who called it fetalization, argued that it was caused by an innate
directional tendency that lacked any immediate adaptive value. This got him into hot
water with critics who otherwise agreed with the sequence of neotenic events in
human evolution that he suggested. To satisfy neo-Darwinism, every separate
anatomical modification must have an immediate adaptive value, scrutinized by
natural selection. It is either that, or a phenotypic manifestation of a genetic unit that
pleiotropically produces a different but adaptive trait, subject to selective approvala
common fallback proposal of mid-twentieth-century population biologists. However,
it is an argument from ignorance unless genetic proof exists. According to Bolk, some
adaptational fine-tuning was ultimately involved, but only after the primary
consecutive or orthogenetic features had been built up in harmony with the whole,
without necessarily conferring an adaptational superiority. In small groups such
innovations would spread by inbreeding.
As late as 1940, Gavin De Beer, in his book Embryos and Ancestors, had no trouble
equating orthogenesis with allometric growth shifts that harmoniously alter the
anatomical proportions of organisms during development. And although it would be
safer for me to do the same, I prefer to recognize the intuitions of the past and retain
the word orthogenesis to represent a larger phenomenon. Julian Huxley referred to
it positively in the first edition of Evolution: The Modern Synthesis (1942), citing pale-
ontological observations of general orthogenetic trends. For example, the trend in
fossil amphibian labyrinthodonts involved flattening and broadening of the head and
anterior body. The skull was shortened, and the bone structure of the anterior cranium
was extended downward, and simplified. These all occurred synchronously in
disparate lineages.5 At the time Huxley warned against excluding adaptationist inter-
pretations of such phenomena, and in his 1962 second edition he came much closer
to Bernhard Rensch and Ernst Mayr. They had taken orthogenesis as no more than the
directional selection of random mutations that affect development.
Orthogenesis 269
Orthoselection was a term coined by Ludwig Plate (1913) for what neo-Darwinists
now call directional selection. According to a personal communication from the
biologist-historian Igor Popov, Plate was a born-in-the-bone orthogenesist who
regarded orthoselection not as a substitute for orthogenesis but as a complement to it.
The story is elaborated by Georgy Levit and Uwe Hossfeld (2006). I argue that some
stages of orthogenesis have no adaptiveness, but there might come a point in the exag-
geration of a trait where it might be distinctly advantageous. Then it would increase
demographically, no longer restricted to the originating lineage. I emphasize that the
increased adaptiveness of the orthogenetic trait results from orthogenesis, and
directional selection is a redundant concept. However, neo-Darwinists argue that
directional selection is all that is required to make a variant that will become a general
population characteristic. If ecological conditions are stable, further exaggerations of
that variation in the same direction will also spread throughout the population. Take
the example of plumage: if the colorful display of a proto-peacock is attractive to
peahens his offspring are likely to be more numerous. Further exaggerations of male
plumage are likely to have a similar effect, so selection of the variation in the direction
of more and more colorful display will go on and on, perhaps to the point of handi-
capping the individual in other respects, such as difficulty in locomotion, and
attracting predators instead of mates.
Exaggerations of the lobate lines in the extinct ammonites can be explained
according to the same logic. These creatures were shelled cephalopod mollusks similar
to the modern chambered nautilus. Their lobate or suture lines mark the septa
between the chambers of the shell. The outermost septum is an interface between the
living organism, in the outer chamber, and the interior, water and gas-filled chambers
that confer buoyancy. The larger the surface area of the septum, the more rapidly salt
and water can be pumped out of the inner chamber, to be replaced with gas. Thus
flotation is increased, and adaptationists are provided with a functional explanation
for the elaboration of the lobate lines. Historically what started out as simple curves in
ammonites became convoluted to foliaceous structures and the clade became extinct.
Then a simple lobate line reappeared late in the era, only to be extinguished along
with all the ammonites by the catastrophe that terminated the Triassic. But no
explanation of ow the lobate line exaggeration was caused was proffered.
Thanks largely to Bernhard Renschs Evolution Above the Species Level (1959), ortho-
genesis was displaced by directional selection. Yet it was cast it away for ideological
reasons, before the molecular basis of heredity was understood. Now, since few
molecular biologists have any sense of history, they have not thought to revisit ortho-
genesis. Modern authors only raise orthogenesis to immediately dismiss it as a
historical fallacy and display how selectionism has progressed beyond such a mistake.
Orthogenesis is one of the many examples demonstrating that, in science, it is
fallacious to suppose (as many people do) that truth must reside in a compromise, or
270 Chapter 7
middle ground, among opposing views.6 This attempts to kill two distasteful birds
orthogenesis and the dialectical synthesiswith one stone.
Often the errors of the old horse evolution exhibit at the American Natural History
Museum are trotted out to discredit orthogenesis. Four specimens had been chosen to
demonstrate an orthoevolutionary trend involving the reduction of toes, increasing
leg length, increase in overall size, and molar tooth specialization. But the pull of the
present was more responsible than the push of the past; i.e., the assumed reality of
direct linear trends resulted in the choice of specimens that would fit, and the actual
irregularity of horse evolution was ignored.7 As G. G. Simpson convincingly argued in
Tempo and Mode in Evolution (1944), the evolution of the Equidae was not linear but
bushy. Simpson disliked orthoevolution and orthoselection for their inelegant
etymologyhe preferred rectilinear evolution. But he did not deny the existence
of such trends.8 Nor did he rule out the possibility that patterns of mutation that were
more likely to go in one direction than any other were a possible mechanism of
rectilinear evolution that could operate independently of natural selection. But he
qualified this by noting that known examples, such as the mutation from wild type to
white eyes in Drosophila usually went against the evolution of the wild population.9
The existence of a directional law of growth independent of natural selection, which
had been acceptable to Darwin was anathema to neo-Darwinism. Now orthoevolution
is taken to be spurious, and orthogenesis a historical fantasy. The pull of the present
is now anti-orthogenetic.
If their premises are accepted, the logic of Simpson and Rensch is impeccable
so much so that selectionists never bothered to suggest any way in which genes
could randomly mutate so as to keep on producing particular trends of phenotypic
exaggeration that directional selection could encourage. Even if the ultramorphosis-
to-extinction argument is dropped, the possibility that a kind of orthogenetic
processa mechanistic, directed allometric growth shiftunderlies directional
selection cannot be ruled out. If so, all such cases would require reconsideration, and
that includes most of organismal diversification.
Where do directional exaggerations come from? Are they due to the selective accu-
mulation of random advantageous mutations, or could the appearance of directional
change through selection pressure mask a more fundamental underlying drive. When
I began to consider the possibility that orthogenesis was a real process, I thought it
irrelevant to evolutionary progress, leading only to more of the same old thing. Intent
on emphasizing emergence to higher levels of organization, I viewed adaptive
radiation, or diversification, as a mere working out of the potential provided by a
major emergence. If you can, like me, but a little bit faster, I hope, detach yourself
from the anti-orthogenetic bias of the Modern Synthesis, start with the notion that
most of adaptive radiation amounts to allometric growth shifts. And then you might
realize that many of them could have been caused by autonomous, self-amplifying
epigenetic mechanisms.
Orthogenesis 271
I should have paid more attention to DArcy Thompson. His book On Growth and
Form had this to say, in both editions (1917 and 1942):
. . . in particular cases, the evolution of a race has actually involved gradual increase or decrease
in some one or more numerical factors, magnitude itself includedthat is to say increase or
decrease in some one or more of the actual and relative velocities of growth. When we do meet
with a clear and unmistakable series of such progressive magnitudes or ratios, manifesting
themselves in a progressive series of allied forms, then we have the phenomenon of orthogen-
esis. For orthogenesis is simply that phenomenon of continuous lines of series of form (and also
of functional or physiological capacity), which was the foundation of the Theory of Evolution,
alike to Lamarck and to Darwin and Wallace; and which we see to exist whatever be our ideas of
the origin of species, or of the nature and origin of functional adaptations. And to my mind,
the mathematical (as distinguished from the purely physical) study of morphology bids fair to
help us to recognise this phenomenon of orthogenesis in many cases where it is not at once
patent to the eye; and on the other hand, to warn us in many other cases that even strong and
apparently complex resemblances in form may be capable of arising independently, and may
sometimes signify no more than the equally accidental numerical coincidences which are
manifested in identity of length or weight or any other simple magnitudes.10
This paragraph would have been more than enough for the Modern Synthesis to
exclude the Thompson transformation theory, since such changes would occur
without reference to natural selection. But Thompson made it worse from the conven-
tional point of view by proposing that there had to be breaks in continuous
transformations, thresholds at which new formulations would apply. And he was quite
satisfied from the evidence of quantum jumps in physicochemical phenomena, as well
as phylogenetic breaks, that saltation was a common mode of evolution:
Our geometrical analogies weigh heavily against Darwins conception of endless small
continuous variations; they help to show that discontinous variations are a natural thing, that
mutationsor sudden changes, greater or lessare bound to have taken place, and new types
to have arisen, now and then.11
In Making Sense of Life (2002), Evelyn Fox Keller asks why Thompson continues to be
mentioned with approval, although his concepts have scarcely helped to advance
biological theory. I suspect that all who look at one of his coordinate geometrical
transformation grids sense that they are missing something important without being
able to put a finger on it. What they are seeing is evidence that doesnt exist for them
because it doesnt fit selection theory. Yet there it is, and Thompson put his finger on
it with complete assurance. His invocation of orthogenesis and saltatory emergences,
and his virtual denial of natural selection, still create the paradox, and guarantee that
he will continue to frustrate all his neo-Darwinist readers.
Straight-line evolution is not inconsistent with divergence. As John Grehan and
Ruth Ainsworth point out in their 1984 essay Orthogenesis and evolution, straight
lines can stop, deviate, and bifurcate. Thus, lines of orthoevolutionreal, or
272 Chapter 7
apparentcan diverge, converge, or run parallel to each other. In Evolutionary Theory:

The Unfinished Synthesis (1985), I included orthogenesis in a comparative table of
several processes that Darwin called laws of growth.12 Now I feel that many of them
could be subsumed by orthogenesis. They are expressions of critical-point emergence,
built upon the interaction of the complementary mechanisms of heterochrony,
organizer topography, and perhaps amplification by some kind of gene drive.
Self-amplifying processes are known to exist, in the form of non-random codon
repetition, non-random tandem gene duplication, and polytene chromosome
production. Some are known to diminish organismal integrity over several
generations, and result in death; but some are also known to be reversible. There is no
reason to suppose that orthogenesis invariably continues until it is detrimental to the
point of lineage extinctionmost molecular mechanisms have off switches. And
there are clearly many living organisms whose distinctive forms arose by non-random,
repeated allometric shifts. Nevertheless, at any stage in its activity, orthogenesis could
be disintegrative, and kill off the organisms that do it. At the risk of flogging a dead
horse, I reiterate that natural selection is superfluous to self-generated destruction. If
adaptively neutral, a novelty will not spread to become a universal population trait,
but will persist in its own descendent lineage, whose numbers will depend on many
other factors. Where it coincidentally confers adaptational advantage the proportion
of its lineage in the species will then increase. Orthogenesis could help to generate
hopeful monsters, which in turn could be the founders of new populations, in new
environments, all with the active orthogenetic mechanism.
I will shortly detail molecular processes relevant to orthogenesis. They might all
contribute to a genetic drive that affects morphogenesis. The implication that these
could be a recipe for orthogenesis was twigged by Jack Heslop-Harrison (1983) and
by John Grehan (1984) before me. But the author of molecular drive, Gabriel Dover,
repudiated the inference, requiring separate evidence for the existence of orthogene-
sis before he would accept that his mechanism had anything to do with it.13
One caveat: While orthoevolutionary trends are evident in fossil series over
geological time, we do not discern major orthogenetic trends happening in existing
wild species. Yet, the molecular mechanisms are hypothetically rapid enough to
produce change from one generation to the next. The leaps of transposable elements
are one example. Another is the pathological phenomenon called anticipation,
which involves orthogenetic amplification of particular codons through replication
slippage, and finally results in ultramorphosis to the point of extinction in the lineage.
However there might be parallel cases with advantageous qualities. In any case, ortho-
genesis might bring about a critical-point emergence and then stop. Or it could occur
early in the lineage of a new clade, reach its characteristic degree of development and
then stop, leaving the new type in a relatively unchanging condition. In other words
it would occur with the punctuation, or even be the punctuation, but not continue to
amplify itself through the equilibrium phase.
Orthogenesis 273
Perhaps we simply cannot see the fossil record with fine resolution, and perhaps
orthogenesis of the anticipation type is too fleeting to be noticed in wild populations.
All the same, orthogenesis can be found at the chromosome level in particular cell
lineages. The polytene chromosomes of Drosophila were a workhorse of research into
the epigenetic hormonal control of gene expression. The question of how the
chromosomes are duplicated and reduplicated without an accompaniment of cell
division has been addressed, but nobody has pondered the other implications. Here is
a cellular lineage, confined to the salivary glands of these creatures, that has clearly
undergone orthogenesis. Related flies with similar life styles do not have the giant
chromosomes, so their relative adaptiveness is questionable, both in incipient and
mature stages. Some insects have polytene chromosomes in their excretory
Malpighian tubules, again without any discernible improvement over their relatives
that lack them. In these examples allometry has been largely confined to particular
organs, has offered minimal advantage, but has nevertheless stopped before becoming
analogous to a cancer.
Moreover, we only need to look through a seed catalogue to find exaggerations of
color and form in cultivated flowering plants. These are not invariably caused by the
supernatural selective action of the horticulturist, i.e., by manipulative hybridiza-
tion. They could be the products of ongoing orthogenetic trends that are encouraged
by inbreeding, while protected from any negative side effects. Indeed, when we
consider domestic animals, such as dogs, allometric shifts are easily detectable on the
scale of a century. Sometimes, in pedigreed lines of animals, the exaggerated traits are
not orthogenetic, but regressive and sometimes dysfunctional. Anyone familiar with
pug dogs, for example, knows how difficult it is for them to draw breath when exerted,
and how susceptible they are to respiratory diseases. Without the ministrations of
their human caretakers they would quickly die out.
Neo-Darwinists might argue that selective inbreeding has flattened the face of a pug
dog, in a manner that is quite clear from paintings of the breed over the last three
centuries. But the exaggerations had to occur before they were recognized. What does
exaggeration mean at the DNA level, and how does it keep on happening?
Convention assumes that non-synonymous point mutation of a structural gene is
involved in directional selection, and that it can keep mutating in a way that
magnifies its original function. As Wallace Arthur (1997) says, the exact changes in
DNA are irrelevant to the formal population model, and, by extension, irrelevant to
neo-Darwinism.14 Yet they are relevant to evolution, and it is difficult to imagine that
point mutations or the exon shuffling mechanisms that Arthur proffers would keep on
producing more of the same instead of something different. Point mutation of a
regulator or a growth hormone gene can indeed affect growth; but could another such
mutation amplify the effect? Most mutations are detrimental, and it is highly unlikely
that any non-detrimental random point mutations would keep producing viable
274 Chapter 7
results consistently in the same direction, as opposed to varying their phenotypic

expressions. Such a mechanism would require a heap more separate evidence or
mystical force than orthogenesis ever needed.
It is much more likely that duplication of a structural gene, or an epigenetic accel-
eration resulting from an alteration in expression of a modifier through dosage
amplification, is at the heart of the matter. At the cellular level of epigenetic induction
of a pug face, a topographical shift of organizer cells produced differential effects,
resulting in a phenotypic saltation distinct enough to attract the attention of breeders.
When they then inbred them to intensify the desired feature, they were allowing the
trend to continue by preventing dilution by cross-breeding. I reiterate that intentional
selection works the opposite way to natural selection, which makes it all the more
desirable to examine how its effects are manifested under conditions where natural
selection is absent. There is no lack of raw data for such a program of analysis.
The non-random nature of orthogenesis at the phenotypic level parallels the non-
random nature of molecular drive, or concerted evolution, associated with gene
duplication. Initial duplications through unequal recombination or gene jumping
may be completely random. But it is known that reduplication affects particular genes,
not any gene anywhere at any time, and some transposable elements have preferred
landing loci for their jumps. Only certain portions of the chromosomes are affected,
and within a species the affected regions are consistent. The differences in DNA
repetition between the domestic mouse, which may have a million copies of a
particular sequence, and related species of mice that only have one, was one of the
first known comparative examples among similar types.15 Finally, amphibian and
fruit-fly studies have found that if repeated sequences are lost, or diminished, they are
replaced in subsequent generations.16
Simple duplications have the immediate potential advantage of functional amplifi-
cation. Whatever proteins those genes code for, every duplication means that the
organism can make twice as much in the same time. In the longer term, repetitive
genes may differentiate, to produce adaptability, or they might cause epigenetic accel-
eration, or the exaggeration of an adaptive feature. Then they might be perceived as
an example of directional selection. Non-random duplications of structural or
modifier genes are not the only candidates for orthogenesis. But these repetitions are
the most obvious way to get large increases in the raw materials necessary for construc-
tion during developmental accelerations brought about by organization changes at
the cellular level.
Most diversification of archetypal body plans is expressed through allometric
growth shifts. Somehow they stabilized before they led to widespread extinction.
Darwin thought that there was a compensation effect, whereby the resources of the
uterus were taken from one region of an embryo and given to another. But a more
likely mechanism is dosage increase by gene duplication, differentially expressed at
Orthogenesis 275
the locus of allometric increase. Since all cells in the body are genetically identical,
molecular governors of DNA operate in the regions where rapid growth is inappropri-
ate, presumably through repression, methylation, or histone regulation. Above the
DNA level there are growth-stimulating and growth-inhibiting factors that affect cell
membrane receptors. Amplification of the intracellular growth cascade system is
another way to intensify and prolong the duration of allometric alterations. Sren
Lvtrup noted in Epigenetics (1974) that allometry is most likely an effect of growth
hormone activity. And although growth hormone gene duplication has been
associated with episodes of rapid diversification in the vertebrates, there are many
other genes involved in growth. The trick is to get the growth localized sufficiently to
produce the allometric shift instead of an overall size increase. Nevertheless, overall
size increase does itself result in allometric shifts, as Stephen Jay Gould pointed out for
the Irish elk. Elisabeth Vrba has numerous examples of relatively sudden universal size
increases in the fossil record of Southern Africa, consistently associated with rapid
climatic change to colder, drier conditions.17 Thus, autonomous drives can be
modulated by the environment.
A hierarchy of epigenetic commands must be invoked before the phenotypic effects
of orthogenesis are discernible. Examples of allometric trends such as anterior
proportions and skull modifications in the ancient labyrinthodont amphibians, cited
by Julian Huxley, may have been associated with environmental changes. But the
more efficient causes were probably alterations in the behavior of neural crest
organizer cells in conjunction with the effects of mutated homeotic genes. Questions
remain: how are these cells freed from tight canalization, and, once free, do they have
a tendency to keep on exaggerating particular novelties in the same direction? We do
know that these things happen, but is it by drive or adaptation? Regardless of whether
a breeder seems to be selecting pugs for their short jaws, or nature seems to be
selecting saber-tooths for their competitive predatory skills, the selection focuses on
organisms in which an epigenetic trend is already under way, and which started and might
continue in the absence of selection.
Paleontologists used to associate orthogenesis with extinction. The allometric trend
became so exaggerated that the final products were unable to survive. In ammonites,
the enhanced buoyancy correlated with increase in the surface area of the foliaceous
lobate lines could have finally been lost because different parts of the septum were
counteractive to the point where the buoyancy mechanism was compromised. Does
their extinction and replacement with others with simple lobate lines indicate an
ultramorphogenetic momentum that natural selection could not stabilize? The male
of the extinct Irish elk Megaceros had massive antlers that were supposedly sexually
selected by susceptible does. But those antlers laid Megaceros stags open to chronic
neck pain, if not increased predation, and offset their sexual advantage. Did orthogen-
esis carry them to their extinction, or was a change of climate responsible?18 In this
276 Chapter 7
case, since the Irish elk survived to leave many fossil remains, the trend to ortho-
genetic doom had probably already been switched off, but although it did not drag it
to extinction, it left it vulnerable to environmental disequilibration. A similar kind of
massive head ornamentation in Rhinoceros has not made it extinctyetthat will
come for entirely different reasons. The dinosaur Triceratops had rococo flanges and
horns that probably conferred some protection.19 Their extinction almost certainly
had an external, catastrophic cause, the K-T bolide impact. But there remains the
possibility that orthogenesis is not only a real, material, heritable phenomenon, but
that occasionally there have been no governors upon it, and it has gone beyond
terminal viability.
Lineages that show orthogenetic trends may diverge because one has briefly
resumed the trend and others not. During horse evolution and diversification,
allometric shifts resulted in the emphasis of a single digit and the disappearance of the
others in the legs, changes in skull and tooth structure, and an increase in overall size.
These affected diverse branches of horse evolution, and taken all together do not
constitute a single continuous orthoevolution of a single trait. Attempts that have
been made to identify such a single line, whether from the adaptationist or ortho-
genetic point of view, are oversimplifications. But the fact remains that the lineage of
modern horses did somehow acquire all of those changes, even if their emergent punc-
tuations were followed by long, periods of orthogenetic stasis.20
The novel variation in an epigenetic algorithm that starts it moving in a particular
direction is by definition a saltatory emergence. Its subsequent harmonious
development depends on both allometric, genetic and epigenetic coordination, and at
critical points functions might change. These processes are independent of natural
selection, but if they keep on in the same direction they might finally reach a
condition that is better adapted, especially if the orthogenetic animal changes its
behavior to take advantage of its changing anatomy. Pierre-Paul Grass (1977)
suggested that orthogenesis could be equated with parallel evolution. He noted how
the evolution of hippomorphs, or horse-like forms, diversified in remarkably similar
trends in the Old World and the New World, and suggested that their common
ancestors already had a propensity to undergo orthogenesis along similar lines. Some
of these problems can now be addressed with reference to deep homology, the
expression of duplicated and differentiated regulatory genes such as Hox, and the
activity of neural crest organizers. But orthogenesis is closer to the actual process than
directional selection.
To earlier generations of biologists the thought of welcoming back the prodigal
principle of orthogenesis would have been intolerable. Bernhard Renschs book
Evolution above the Species Level (1959) was devoted to the thesis that the origin of
varieties within populations was the same process as that leading to speciation, and all
points beyond. However, the replacement of orthogenesis by directional selection was
Orthogenesis 277
not a matter of a demonstrably faulty explanation being supplanted by one based on

more rigorous evidence. Here, a majority opinion prevailed without reference to any rational
evidence at all. Michael Ghiselin, in a recent personal communication, counters this
with the opinion that the internal self-amplifying drive was rejected not for
ideological reasons, because it would make natural selection redundant, but because
there was no reason to invoke it. I would think that the proven existence of self-
amplifying drives more than sufficient reason to invoke them. It was such a
dialectically successful attack on orthogenesis that, malgr Grass, modern molecular
biologists and some students of body plan evolution now deal with the process
without being aware of either the term or its morphogenetic implications. I must note
an exception in Keith Thomson who mentions it as orthogenesis, before substituting
the term trends. In Morphogenesis and Evolution (1988) he writes:
Their most obvious explanation would be causation through strong and historically consistent
external directionality of selection. However, it is also obvious that many evolutionary trends
also have a strong internal generative aspect. An obvious example would be any trend in shape
that was driven by allometric size change. Some aspects of horse skull evolution are the direct
consequence of increase in size. Size increase then is the real trend, and skull shape and
proportion merely follows. But, as MacFadden (1986; cf. Radinsky, 1984) has shown, the early
part of the history of horse evolution was accomplished in the absence of major size increase.
Therefore, it is worth asking whether evolutionary trends may have some other deeper, internal
cause.21
Although Thomson then argues that size increase per se could fit the directional
selection model, he has to assume that there is a generating mechanism in place to
give selection something to work with. As a variation on the theme he adduces devel-
opmental constraints. Such constraints might apply asymmetrically, so that some
proportions of a limb, for example might elongate, while others did not. Then
Thomson suggests that many different genetic variations, introduced at different
levels in the morphogenetic cascade, could combine under this integrative influence
to cause phenotypic changes in the form of a trend.22 Call it trend or call it ortho-
genesis; however many diversifications have occurred, each of its products had its own
lineage. Its track might be lost among the bushes, but it is there, and more likely to
have been produced by orthogenesis than directional selection.
I have already pointed out how difficult it would be for a series of random point
mutations of a single gene to produce an orthoevolutionary series of phenotypic exag-
gerations. But it can always be argued from ignorance that every trait is determined by
multiple gene interactions, and that hypothetically there could be an astronomical
number of combinations from which directional selection could produce an apparent
trend, every stage of which is progressively fitter. It still doesnt get around the
fundamental problem of the non-fitness of incipient stages. And recombination is
always a difficulty for precarious combinations. Thomson is sufficiently troubled by
278 Chapter 7
the phenomena of parallel and convergent evolution in disparate lines of cloven-

hoofed and single-hoofed ungulates to insist on a generative developmental
mechanism, rather than leaving it to directional selection alone. Such mechanisms
must represent the inverse of developmental constraints. They are not predictable
from a study of individual genes and gene expression and, except at a phenotypically
trivial level, neither predicted nor explained in terms of population genetics.23 I think
he is ready to run away and join the circus.
In The Shape of Life (1996), Rudolf Raff just dismisses the idea that orthogenesis
exists, using the oft-cited example of bushy rather than orthoevolutionary trends in
horse evolution, but he echoes Keith Thomson when he writes:
Although the idea of internally directed evolution is not tenable, the potential role of internal
factors or constraints remains a viable one even in a selectionist context. Existing genetic and
developmental systems are not neutral features, nor are they necessarily readily dissociable.
Existing developmental systems must produce constraints on the degree of freedom with which
selection can operate. Thus, a major principle of evolution exists beyond an all-powerful
selection working on randomly generated variation, and the inner workings of genetic regulatory
systems and developmental processes as well as their histories must be considered as key
elements of evolution.24
Rightas far as it goes! If an organisms development is so tightly canalized that only

one alternative avenue of development remains unconstrained, that will be the
avenue taken, and the result will be orthoevolution. It will continue for as long as the
lineage is exposed to the triggering stimulus, and natural selection will have no role
in its generation. If they were to entertain the untenable a little more, epigeneticists
such as Raff might want to take a closer look at molecular mechanisms that produce
the same kinds of effects, regardless of developmental constraints and natural
selection. Orthogenesis merits a significant place in the ranks of evolutionary causes,
and it would be worth re-examining every case of directional selection for an ortho-
genetic component.
Genetic Drive, Allometry, Anticipation, and Orthogenesis

For the phenomenon of self-amplifying repetitive differentiation at the molecular
level, I have suggested the term genetic drive, which involves any non-random self-
amplifying genetic change, such as gene duplication, mutational repetition and
concerted evolution. As Britten and Davidson argued in 1969, duplication of particular
genes seems to keep on happening regardless of adaptiveness or natural selection.
Selection would only have a limited metaphorical role in culling any that show dosage
imbalance, which could waste energy and adversely affect the availability of amino
acids and nucleotides for essential syntheses. Selection does not cause the buildup of
multiple genes, but where products of gene drive coincidentally show a pronounced
competitive superiority, the proportion of organisms that possess the drive will, of
course, further increase in the population.
Orthogenesis 279
I have applied the concept of repetitive differentiation to the development of

biochemical adaptability, where a suite of proteins can meet the demands of a varying
environment. Here highly concerted molecular evolution would be counterproduc-
tive, since the range of variation within the individual organism has to be preserved
to afford adaptability. To be effective there would also have to be further adjustments
to the regulation of the duplicated genes, so that in the case of salmonid kinases the
activation of the appropriate genes would be sensitively set to narrow temperature
ranges.
The distinct trends in allometric growth shifts that have been associated with ortho-
genesis in the past cannot simply be explained by exon or gene duplication per se,
although this kind of DNA repetition does suggest how growth might be accelerated.
There has to be an additional regulatory mechanism, involving, for example, a growth
hormone. During morphogenesis it might react with larger numbers of receptors in
specific organs, or stimulate a greater amplifying cascade of second messengers in the
affected cell lineages. Or there might be a more profuse synthesis of the effector
enzymes that respond to the growth stimulus. Tissues that are being allometrically
enhanced need to grow faster, and their cells need to divide faster, but in a manner
that can be accommodated within organismal integrity, rather than like a cancer.
Recall also that allometric growth may require more than simple tissue growth accel-
eration. Taking the example of the giraffes neck once more, not only does there have
to be an increase in the rate of growth and elongation of the cervical vertebrate and
associated tissues, this also has to be achieved in the entire front quarters, including
the pectoral girdle, legs, heart, blood vessels, and nerves. A simpler example relates to
the allometric growth of feathers. Minimally this requires the interaction of the genes
sonic hedgehog and bone morphological protein 2 in promoting cellular proliferation and
differentiation. But these genes participate in many anatomical processes, their role in
bony facial structure, tooth and beak structure among others. For them to work
effectively in feather epigenesis they have to be expressed in the right place at the right
time and the right rate, in conjunction with regulatory factors, such as modifier genes,
and neural crest cells. To work, allometric shifts have to be not only harmonious with
other patterns of growth, but also directional. Self-amplificationorthogenesisis an
effective way to achieve this, provided there is also an off switch.
My question for selectionists is this: Does any directional evolution rely upon
natural selection acting on random mutation? Hypothetically it could result from
genetic drive, local proliferations enhanced by gene duplication, or induced by
epigenetic mechanisms at a cellular level that coincidentally give a competitive edge.
Individuals with dosage imbalance would fall by the wayside in any case, through
failure of organismic integrity. This seriously challenges the one kind of natural
selection that even dissidents regard as evolutionary. I am perhaps overcomplicating
allometry, since it can sometimes arise from size changes alone. Aside from these,
280 Chapter 7
embryonic canalization might only allow alterations in a single developmental

direction. In that case, allometric shift must always be directional, without the
necessity of directional selection.
As an analogue of orthogenesis, the pathogenic condition known as anticipation
is instructive. It was first known from myotonic dystrophy, a muscular disfunction.25
More recently its genetics have been investigated for Huntingtons disease, and for
mental retardation caused by fragile-X.26 The most general observation made about
these diseases is that they were genetic, and that it could be predicted that they would
worsen from generation to generation. The word anticipation suggests predictabil-
ity, but actually means that in subsequent generations the onset of the condition
becomes progressively earlier, as well as more severe.
Myotonic dystrophy was initially detected from cataracts in elderly but mildly
affected sufferers. The condition would worsen in subsequent generations to the point
where cataracts would affect the middle-aged, and then muscular symptoms in the
young. The history of the major lineage of myotonic dystrophy has been traced to a
single triplet duplication about 300 years ago.27 Since only one codon is concerned,
and it occurs during mitosis and meiosis, replication slippage is believed to be the
initiating molecular process, although unequal crossing over could be significant in
extreme cases.
Fragile-X is named for its cytological phenotypic expression: breakage of the X
chromosome due to heavy methylation at the locus of FMR1. At the genotypic level
there are duplications of the base triplet coding for arginine. In the population at large
up to 54 duplications can occur, without any phenotypic manifestation of the
condition, nor any detriment to offspring. Between 52 and about 90 repetitions of the
triplet is the normal transmitting condition where there is no initial phenotypic
expression but the parent can be considered a carrier. From here it can be predicted
that fragile-X will be phenotypically expressed, with an average of 10 duplications
added per generation. However, regression is also known. Transcription from the
strongly affected gene to messenger RNA is inhibited.
There is nothing speculative about the fact that anticipation at the level of
molecular processes is exaggerated by an autonomous, self-amplifying driving
mechanism. It is orthogenesis by another name. Natural selection qua differential
reproduction has no part to play in its progress, which in the case of anticipation leads
the lineage to a self-eliminating, detrimental condition. As I have argued before, it is
redundant to adduce a metaphorical undertaker to reach a fate that was implicit in the
generative mutation. If a pathogenic condition can proceed orthogenetically at such a
speed, one that starts out in a selectively neutral state might progress even longer
through genetic drive, and ultimately display beneficial qualities under the prevailing
conditions, with the option of stopping, or going on to eliminate itself through
detrimental hypermorphosis. The action of natural selection is irrelevant to these
events.
Orthogenesis 281
Gabriel Dover (2000) writes that he regrets coining the expression molecular drive,
since it suggests a deterministic qualitydespite his acceptance of natural selection as
a deterministic, non-random product of selection pressures arising in the
environment.28 If he were simply to equate his drive with any autonomous self-
amplifying molecular process he would not have a problem, especially since he goes out
of his way to demonstrate how such processes occur without reference to ultimate
reproductive success. Two examples that he gives are the proliferation of segments in
snakes and centipedes through the repetition of identical Hox influences. Segment pro-
liferation is a lavatory-roll model of evolutionidentical bits keep coming and
coming. Although Dover (1982, 1986, 2000) does not mention orthogenesis within
molecular drive or TRAM systems (q.v. previous chapter), he asserts that these kinds of
processes are directed only in certain gene families and are not random, in contrast to
the effects of natural selection and genetic drift. He is really writing about orthogenesis.29
Dover (2000) also describes another self-amplifying genetic drive phenomenon
involving a jumping gene called P-element. Dovers P-element was accidentally passed
from Drosophila willistoni to D. melanogaster by a parasitic mite. In the new host, the
effect was sterility through chromosomal disintegration and gonad destruction. Once
established in a chromosome of the new host it was replicated during mitosis, so that
the homologous chromosome in the cell lineage came to possess it as well. Part of the
single transposable element codes for a transposase that triggers the jump. When it
jumps, the gap it leaves is filled by a new copy induced by the non-transposing
element in the other homologous chromosome. The self-amplifying DNA is then
spread through the population by sexual reproduction. Coincidentally, in populations
that were not driven to extinction through sterility by P-element, several compensat-
ing mechanisms had appeared. One of them inhibited the effect of the transposase,
and so prevented the jump. Another was a repressor protein that enhanced the repro-
duction of the individuals that possessed it. Any compensating mechanism that
appears will save the day. Therefore it is redundant to say as Dover does, that it is
seized on by selection to overcome the debilitating effects of hybrid dysgenesis.30
Spiegelmans Monster is also relevant to the orthogenesis v. directional selection
debate. This is the name sometimes given to the subject of A Darwinian Experiment
with the Replicating RNA Molecule. It refers to a viral RNA strand that over a period
of time showed reduction in size and increase in replication rate, and the research is
reviewed by Spiegelman (1967). Denis Schwartz communicated his view that it was an
orthogenetic process, noting that no one had challenged the Darwinian label. Paul
Davies (1999), however, treats it, along with Eigens work on the self-assembly of RNA
strands from a solution of simple ribonucleotides, as a model for Darwinian evolution
at the molecular and possibly prebiotic level.31
The starting components of Spiegelmans experiments were RNA strands from a bac-
teriophage virus, an RNA replicase that could recognize them, and ribonucleotides
282 Chapter 7
that the system could use to build the replicates. Over a series of 75 reactions, he
regressed the time allowed for the process, and transferred a portion of the reaction
products to the next stage. He was deliberately selecting the fastest replicating and
smallest products. After the fifth transfer the viral strands had lost their biological
competence, i.e., they could no longer act as infectious viruses. By the final transfer
the strands were reduced to 17 percent of their original length and the growth rate was
fifteen times faster than that of the original viral molecules, and still recognizable to
the replicase.
This is unequivocally an exercise in artificial selection. Factory farming tries for the
same rapid production of stock, though attempts to increase size are usually more
common. In any case, competition from slower growing RNA strands was removed,
and the selected molecules were given unlimited resources and protected from the
biological consequences of over-simplification. As to orthogenesis: the RNA strands
seem to have had a self-reducing characteristic that the experiment allowed to
continue beyond the biological point of no return. This had to be present before it
could be selected. In nature such a process would be masked by the complexities of
the virus and its host, and also be self-eliminating, unless the self-reducing strands
took up a permanent parasitic existence in the host bacterial cell.
Dwarfs and Giants

The discovery of the fossil remains of Homo floresiensis, putatively a dwarf strain of H.
erectus, has reawakened interest in evolutionary trends toward dwarfing and giantism
among island fauna. Examples from Flores Island in Indonesia include komodo
dragons (giant Varanus lizards), pygmy elephants, giant rodents, and dwarf
hominins.32 Overall size increase could be explained as a saltation due to a growth
hormone gene mutation, or an orthogenetic trend involving the amplification of
growth hormone and its receptors. Dwarfing is unlikely to be due to a negative ortho-
genesis, simply a heterochronic epigenetic change. Here a saltatory phenotypic effect
is more likely to be the effect of an epigenetic change that cuts growth at an early
stage. The same may apply to the example of the reduction of the snout in pugs.
Traditionalists struggle to explain these effects in terms of the gradual natural selection
of random point mutations. But when an organism finds itself on an island with any
kind of useable resources the agents of natural selection, i.e., competition and
predation, are diminished or absent. Other things being equal, it doesnt matter if the
organism gets huge or tiny provided it maintains its integrity. There may be no
particular advantage to either until the hypostasis of natural selection is imposed by
increased competition.
In conclusion, Mivarts supposition that the laws of growth were due to innate
tendencies were certainly true in as far as divergent lineages would still have the
majority of their epigenetic inheritance systems in common, and that the same rules
Orthogenesis 283
of constraint would likely apply after divergence. Beyond that, self-amplifying systems
also represent innate tendencies that operate within the rules of constraint, but
produce novel allometric shifts, regardless of the relentless demands of selection
pressures.
Postscript
While I was preparing the final draft of this chapter, there appeared a most interesting
and challenging publication by John Fondon III and Harold Garner: Molecular
origins of rapid and continuous morphological evolution (2004). It deserves
particular attention, since it bears out David Kings suggestion (q.v. chapter 6 above)
that tandem repetition of codons need not be pathological, but could be a useful
source of variability. Since it also suggests a more selectionist-friendly interpretation of
phenomena that I would treat as orthogenetic, I review it here. First, I repeat their
remarks that are most supportive of my position. Rapid and continuous evolution
speaks for itself. They report a consensus among molecular geneticists that random
point mutation is insufficient as a source of variation for natural selection to be
effective, and that mutations in cis-regulatory elements are the predominant source
of the genetic diversity that underlies morphological variation and evolution.33 In
their study of the evolution of domesticated dogs, the mutations are tandem codon
repeats within such modifier genes as Alx-4, Runz-2, Twist, and Dix-2. They modify the
production of proteins with runs of glutamine and alanine, for example. These
proteins participate in the epigenesis of craniofacial features, limb length, and digit
number.
Tandem repeats within regulatory genes are always involved in the epigenetic
changes under discussion. Fondon and Garner note a correlation between allele length
(as determined by the number of repeats) and the size of a phenotypic character. Point
mutation rates are far too low to provide dog breeders with enough variation from
which to select. In contrast, increased codon repetition, as well as deletions, provide
for gross morphological novelty, reminiscent of the saltatory genetic events
Goldschmidt envisioned for his hopeful monsters.34 Especially interesting is their
conclusion that what in the case of anticipation is pathological, is in far more cases in
nature a potential for viable evolutionary change.
More controversial for me is their inference that the evolution of dog breeds is
driven by the breeders selection of particular features; that tandem repetition and in
some cases deletion of repeats occurs rapidly enough to allow for the historically rapid
changes in dog features. Extending their study to other canids and a variety of
mammals including otters, walruses, rabbits, bats and humans, they find similar
repetitions in the same kinds of epigenesis-modifying genes, and conclude that in
these cases the divergences are driven by natural selection. I will only comment that
284 Chapter 7
these are in part products of orthogenetic self-amplification. They are initiated neither
by artificial nor natural selection, and they proceed until the breeders notice that there
is something new from which to breed, or until an advantageous quality for their
conditions of life helps the mechanism to spread. As Grehan and Ainsworth (1985)
point out, direct lines of evolution can branch and go in different directions, so ortho-
genesis can be a significant part of diversifying evolution, whether within the
domestic dog species or within the entire taxon of placental mammals.
Where Are We?
In the prologue to chapter 2, I submitted a field-trip checklist for the visit to the causal
arenas of emergent evolution. This was updated at the end of chapter 3, at the end of
chapter 4, and at the end of chapter 5. We are now in a position to add epigenetics
and orthogenesis.
1. Mechanisms that perform in all the arenas of emergent causation.
The prominent mechanism is repetitive differentiation, applying to molecules,

segments and organs. To stretch the point it could also be applied to social insect caste
systems, and human manufacturing activities. Simple gene duplication or dose ampli-
fication may precede differentiation at the molecular level and contribute to
allometric growth and orthoevolution.
Modular shuffling of exons, combined with mutations of the receptor sites in
promoters, and the consequent increase in their algorithmic complexity universally
affect developmental changes. Transpositions of genes have also been important in
epigenetic evolution. All of these have effected not only developmental evolution, but
also, as a consequence, physiological and behavioral evolution. Major adjustments to
symbioses have also been effected by gene jumping.
Environmental stimuli have directed specific epigenetic changes. Physicochemical
physiogenesis has also been generally affective. Physiogenic changes have often been
internalized to consolidate homeostasis and homeorhesis.
Retroviral and bacterial transgenesis potentially affects all molecular causal
mechanisms.
Marguliss principle of mixing and matching applies not only to the generative
conditions for symbiosis, and biochemical rearrangements between host and
symbiont. At the molecular level, the same applies also to processes of topological and
sequential gene and protein rearrangements, and shifts in reading sequences. While
much of adaptational evolution may be driven by particular and persistent organismal
actions, the molecular laboratory in the basement, even operating at random, has a
huge capacity to come up with experiments that will accommodate those actions.
Orthogenesis 285
2. Generative conditions from which emergences spring and common features of

effective generative conditions.
The holonic, or modular, nature of life, which involves the reproduction of hierarchi-
cally arranged units is a major generative condition of developmental, biochemical,
physiological, anatomical and behavioral complexification and diversification.
Especially important was the establishment of cellular modularity in multi-cell
organisms. The concurrence of efforts is easier if the separate offices are close to each
other.
The generative conditions for some complex organs like eyes and appendages are
universal, making their emergence highly probable, under appropriate organismal
conditions, as illustrated by the number of times they have independently emerged.
Yet these independent emergences are also dependent upon the deep homologies
provided by homeotic genes.
Conditions conducive to epigenetic evolution often involve developmental nodes
or thresholds, as well as changes in gradients leading toward those thresholds.
Environmental gradients and thresholds (or interfaces) are among the generative
conditions for symbiosis. At interfaces, the prolonged concentration of different types
of organisms with a potential for sharing their talents is a good way for the unlikely
to become the likely.
Such gradients and interfaces also affect physiological and behavioral evolution.
They sometimes allow respite from the agents of natural selection. But while environ-
mental gradients and interfaces physiogenically altered the internal milieu of simple
organisms, the provision of a stable internal milieu was to become a generative
condition for many emergences. Cellular environments had to be stable enough to
allow eukaryotic endosymbiosis. The emergence of viviparity provided constancy for
the fetus prior to birth, and in placentals was a generative condition for the success of
offspring whose own homeostatic mechanisms were late-developing. The more stable
the internal milieu, the greater the capacity of the type to diversify (anatomically, by
orthogenesis) after passing through environmental thresholds.
The emergence of any kind of adaptability potentiates further evolution through
extending the ability of the organism to try new behaviors and environments whose
influences reverberate through all of the causal arenas.
3. Key innovations that catalyze emergence, provided that other appropriate

generative conditions are present.
Major ones are early biochemical acquisitions such as photosynthesis, and sulfur-
oxidation; structures such as chromosomes. waterproof insect integument, and
neuron myelination; cleidoic eggs, feathers, and parabronchi in birds; and hair,
286 Chapter 7
placentae, and neopallia in mammals. The multiplicity of examples makes generaliza-

tion daunting, but they often involved epigenetic change and enhanced physiological
and behavioral adaptability.
4. Particular contingencies, predictable or unpredictable that have affected generative

conditions.
Disequilibration of homeorhesis and homeostasis by environmental effects was a

necessary generator of emergence in early epigenetic and physiological evolution.
The availability of environments that could have these effects is predictable for any
Earth-like planet with seas and continents and plate tectonics.
Concentration of adaptable plants and animals, metaphorically at the edge of chaos,
or actually at the interfaces between environments where competition and predation
is reduced is also predictable.
Physiogenesis resulting from environmental shifts is a predictable matter of physic-
ochemistry.
Catastrophic extinctions and physiogenic effects of bolide impacts, and volcanic
action remove the agents of natural selection and lead if not to direct emergences of
adaptable organisms, then to the demographic success of those already in place, and
their rapid diversification.
5. The constellation of multiple functions characteristic of new emergences.
While they differ from one example to another, multifunctionality is a common

attribute of emergent systems. Simple epigenetic changes such as alteration of egg size
or reduction of photoperiod can cause paedomorphosis with multiple effects. Simple
increase in size causes allometric shifts.
Changes that increase adaptability are virtually synonymous with multiple func-
tionality, and they occur in all the causal arenas. The problem with the selectionist
explanation is that it sees only one feature among many that it ignores.
6. The course of emergent evolution that has progressively led to greater self-organiza-
tion, independence and freedom of choice.
At different times in the history of evolution symbiosis, association, epigenetic differ-

entiation, physiological adaptability, behavioral freedom, have interacted to send out
waves of progressive change that generated new major emergences. Bootstrapping
says it more succinctly. Orthogenetic/allometric shifts in the central nervous system
have been an integral part of several independent animal lineages, with the most
dramatic found in the primates. While chronological priority is easy to establish, it is
Orthogenesis 287
impossible to rank the causes of emergent evolution in order of importance for evolu-
tionary progress.
7. Emergent evolution and adaptive radiation.
Although the emphasis of this book has been on progressive evolution, this synopsis
would be incomplete without reference to the diversifying evolution that results from
major emergences. This chapter has demonstrated the feasibility of self-amplifying
processes responsible for allometric shifts that are key to anatomical diversification.
Indeed the question has been raised if the concept of directional selection is necessary
for anything but the simplest adaptational changes. Allometric shifts, which may be
subject to strong epigenetic constraints, exemplify critical-point emergences, and are
subject to behavioral adaptabilities Can the organism work with the shift? Or is it
capable of changing its behavior to suit?
It should be remembered that regressions occur on the way to specialization, again
limiting the organisms functional options. Yet some developmental regressions such
as paedomorphosis can be keys to escape from specialization.
8
The Re-invention of Emergence
The distinction between sums-of-parts (or aggregate) and structural characters is crucial to
biology: if new and nonaggregate structure had not emerged at various times in the history of
life, neither the tiers of lifes hierarchy nor selection at these successively higher levels of organ-
ization would ever have evolved.
Elisabeth Vrba, 19891
The vast mystery of biology is that life should have emerged at all, that the order we see should
have come to pass. A theory of emergence would account for the creation of [that] stunning
order. . .as a natural expression of some underlying laws. It would tell us if we are at home in the
universe, expected in it, rather than present despite overwhelming odds.
Stuart Kauffman, 19952
[The big questions are about] causes, strengths of causes, levels of causes, and contingency. Thats
not a bad formulation. . . . The emergent property is the emergent property, and thats all you
can ever say about it.
Stephen Jay Gould, 19963
Emergence wants re-inventing for several reasons. First, the old concepts have been
largely forgotten, along with their emphasis on spiritual emergents that transcended
biological realities. Second, its re-invention might relieve the current sense of unease
among some evolutionists. Third, biologists already treat emergent phenomena with
easy familiarity, and are likely to be receptive to a formal treatment. But there remains
a need to explain how emergences are generated and why they matter. Elisabeth Vrba
says that as non-aggregative structures they have been essential for evolution. Stuart
Kauffman expects an emergence theory to state the underlying laws of the creation
of orderthereby explaining progressive evolution. Stephen Jay Gould challenges us
to find more to say about the emergent property than that it simply exists.
Kauffman, like most complexity theorists, is on a grail questfor a simple formula
that would apply equally well to physicochemical phenomena, the emergence of life
from heterogeneous mixes of autocatalytic molecules, or to the emergence of new
levels of organization in multicellular organisms. Fittingly, he uses the plural,
290 Chapter 8
underlying laws, because there are more than one, and they do not lie only at the
physical foundations, because each new emergent level manifests a new set of
overlying laws. Therefore emergence implies discontinuity. And although the current
literature is still prejudiced against the word saltation, it would, by any other name,
be just as jumpy, even in cases where the generative conditions have varied continu-
ously. For example, when dealing with change in non-living, dynamically stable
systems, complexity theorists use bifurcation to signify the emergence of sudden
and dramatic changes in trajectories and attractors.4 Another fundamental aspect of
emergent evolution is that it often arises from organizational changes in hierarchical
systems, something that its early proponents perceived but did not analyze. To explain
it in that context is a major challenge to modern emergentists.
In chapters 47 I brought together some of the pertinent biological information,
detailing the programs of performances staged in the various causal arenas. Now we
need to transcend the circus metaphor to bring in hierarchical structures. We can
approach the problem of understanding evolution at any level in a biological
hierarchy, provided that we are willing to move up to the highest levels as well as
down to the lowest, without judging any one of them as more significant than any
other. Physiologists do that without even thinking about it. Unfortunately, much of
conventional biology that doesnt stubbornly stick at the population level plummets
to the genetic basement. The epigenetics department is attracting greater numbers, but
the physiology mezzanine is largely deserted.
I will begin this chapter with a more comprehensive statement of the definition of
emergence that appeared in the introduction and in chapter 2: Emergence is the
spontaneous appearance of novel qualities through the interactions and constraints of
generative conditions, consisting of the dynamic structure of the original, and
properties of its environment. Thus stated, emergence includes a wide range of
physical events from the Big Bang to the physicochemical reactions that produce
liquid water from hydrogen and oxygen at appropriate temperatures and pressures. It
also allows for the introduction of a catalytic factor. And it assumes physicochemical
and biological constraints on natural experimentation. Evolutionary emergences
normally depend upon a genetic foundation and its reproduction to see them through
to the next generation. But there are intermediate biological emergences that are
effected by environmental conditions that may persist for many generations. Until
such time as they are genetically assimilated they are not biologically reproduced.
They are simply always present as part of the generative conditions. In that sense they
are innate in the broad usage of Susan Oyama (1985) and William Wimsatt (1998).
Now I will pick up the patchy history of mechanistic attempts to grasp emergence,
and survey the thoughts of biologists who have portrayed it as an independent
generative process of evolution. Some Modern Synthetists have acknowledged its
importance, while subordinating it to the ultimate mechanism of natural selection.
The Re-invention of Emergence 291
Following a round up of others ideas, I will delineate intrinsic and extrinsic events
and their saltatory or gradual gaits.
Emergence after Morgan
Emergence is to me the obvious choice of name for a process competent to leap the
barriers of ecological, organismal, and theoretical stability. Thus stated, the concept
challenges the causal gradualism proposed by neo-Darwinism. It modifies and builds
upon C. L. Morgans Emergent Evolution, which has an honorable if largely forgotten
past. In Evolutionary Theory: The Unfinished Synthesis (1985), I discuss Morgans work
extensively, and therefore kept my chapter 2 outline brief. The concept is unpreju-
diced as to the sources of evolutionary changes, whether they be genetic, epigenetic,
associative, physiological, behavioral, or environmental. It has been perennially
perceived as innovation in any of those arenas. My emphasis has, however, been on
changes that establish multifunctional, adaptable properties. Such novelties can arise
in a variety of ways from any level in the hierarchy of life:
at critical points (or thresholds) in continuities of change
from a complementarity of previously unassociated systems
by radical autonomous re-organization
though the complexification of existing regulatory dynamic structures
by simple mutations that advance adaptability
from the organisms actions
from the environments effects and the organisms reactions.
This, however, is getting ahead of the game, since Morgan did not attempt a serious
analysis of emergent processes. Nor did Arthur Lovejoy, pioneer of the history of
ideas. However, his essay The meaning of emergence and its modes (1927) set out
the range of qualities that characterized emergences, excluding transcendental
processes such as vital sparks. I have here rearranged his list of the qualitatively
different kinds of emergences that might occur in evolution, in descending order of
importance5:
l. New events irreducibly different from old ones.

292 Chapter 8
2. New types which have some new qualities and may lack some old ones.
3. A new quality in a pre-existing organism.
4. An improved method of doing the same general thing.
5. Proportionate numerical increase.
Lovejoy did not intend this is to be an ideal table of mutually exclusive categories, and
it covered the bases so widely that almost any biological change could be labeled an
emergence. But he gave us the first materialistic, analytical approach to emergent
evolution. May we take it from the bottom?
The least category, number 5, includes natural selection as differential survival and
reproduction. Since, at the molecular level, structural DNA mutations are all-or-
nothing saltations, they would also be considered emergences, but their consequences
might be merely neutral or adaptationalimproved methods of doing the same
general thing, as in category number 4. Progressive steps in the evolution of adaptabil-
ity, or self-organized integrity, could also come in at this level. They might be just as
important as some processes at the top of the table.
Number 3new qualities in old organismswould include the physiogenic changes
in fish migrating back and forth between the sea and fresh water, and the
development of lungs in stagnant-water fish, or wings in reptiles, or all of the familiar
divergent homologies of placental mammals, as well as mechanisms of allometry and
orthogenesis.
Under item 2 there are any number of archetypal novelties of plants and animals,
poised to invade new environments or dominate the old, and to diversify widely as a
result of their emergence.
Number 1new eventsare exemplified at the primordial functional level by
sexual reproduction, or at the organismal level by the symbiotic emergence of
eukaryotes. The major emergences of life and mind would top the list.
Emergence through the Looking Glass
Ernst Mayr
Adaptation and numerical increase, the least of Lovejoys categories, have drawn
almost all the attention that selectionists have given to specific cases of evolution for
the last century. However, Ernst Mayrs 1960 essay The emergence of evolutionary
novelties took a broader view. Since some modern biologists still cite it as the author-
itative word, it deserves further scrutiny.
To keep emergence in safe hands, Mayr proposes that Darwin had already
anticipated it, although it had surely been greatly neglected during the past two or
three decades, in spite of its importance in the theory of evolution.6 Mayr subse-
quently denounced all of the saltationists, essentialists, typologists, and hopeful mon-
strologists who had not neglected emergence. Notwithstanding, his earlier essay
established the selectionist view of emergence, and shows insights that were not
blinkered by its conventions.
Evolutionary novelty gets the working definition of any newly acquired structure
or property which permits the assumption of a new function.7 Although Mayr
remarks that biochemical novelties based on a single gene mutation are more likely to
confer the quality of general adaptation (which I would call adaptability), he
mainly discusses structural novelties that represent adaptation to a more specialized
situation.8 Here follows a brief summary of what Mayr takes to be the causes of the
emergence of novel structures, along with my comments in brackets:
l. Pleiotropic by-product: a secondary, neutral phenotypic feature of an existing gene

acquires selective value. [Or, a hitchhiker takes the drivers seat. Where the expression
of a gene contributes to several phenotypic features it is said to be pleiotropic. To an
epigeneticist, the earlier a gene participates in development, the more pleiotropy
would be involved.]
2. Intensification of function. An example is the intensification of the locomotory

function of a limb that leads to specialization for high-speed running. In artio-
dactylescloven-hoofed animalsthere is no radical innovation but an improvement
in the mechanical efficiency of a tarsal joint. A small structural change makes drastic
reorganization of the phenotype possible. Moreover, such improvements can lead to
an evolutionary avalanche. [Mayr does not, however, address the cause of the
allometric shift in the growth of the limb, or the trend toward epigenetic emphasis of
a single digit, or even ontogenic anatomical modifications that result from behavior.
And although these are not radical innovations either, they would seem to be more
central to this intensification of function than a joint modification. This category
comes under critical-point emergence.]
3. Change of function. This includes duplication of an organ, and variation of function.

The same effect can come from extension of an organ and its subdivision into two
areas with different functions, as in a digestive system. There is always a transitional
stage during which both structures function simultaneously, e.g. the changes from
ovipositor to sting, jawless fish endostyle to thyroid, scales to teeth, and leaves to
petals. A final type of functional change is one where an existing structure is
preadapted to assume a new function without interference with the original
function.9 [This brings in multifunctionality, a common emergent property; for
example, body surface vascularization serves variously for respiratory gaseous
exchange, heat absorption, and cooling. But these come into play simultaneously at
the point of emergence.]
294 Chapter 8
So far I find little to disagree with, although biochemical adaptability has been given
short shrift, multifunctional adaptability is put down to preadaptation, and perish the
thought that orthogenesis could be a process of intensified function.
Mayr also emphasizes the role of the environment and the behavior of the
organism. Ongoing minor changes in large environments were unlikely to be of major
importance, though broad adaptation [ = adaptability] was likely responsible for
success in the face of such change. I take the contrasting position that specialization,
regression of adaptability, and ecostasis are the most likely products of dynamically
stable environments. A small pool of adaptable generalists will persist if periodic
changes are sufficient to give them an occasional break from the usual restraints of
selection, although their fitness will usually be low relative to more specialized
variants.
Mayr gives some credence to this point of view by citing certain songbirds of the
Oscines genus. Among them, the omnivorous generalists have relatively large brains,
while specialists are more typically bird-brained. In his work on the plasticity of the
song control system of birds, Eliot Brenowitz is more specific. The brain nuclei in birds
that have a greater adaptability to learn new songs into adulthood, are capable of
seasonal expansion.10 According to Mayr, a phenomenon of even greater significance
occurs where the active shift of an organism into a novel niche or entirely new
adaptive zone will set up a powerful array of new selection pressures. An organism
must have a special set of characteristics to cope with the demands of the new
environment. It must be preadapted for the new world in which it will henceforth
live.11 Mayr goes on to remark: Perhaps most astonishing is the relative slightness of
reconstruction that seems to be necessary for successful adaptation to rather drastic
shifts of adaptive zones.12 It is not astonishing to a physiologist, who might be more
aware that physiological adaptability gives the occupants of interfacial environments
the potential to cross over, and to experiment with various behaviors. Morphological
change is initially a minor consideration. New selection pressures are supernumerary
since the adaptability is already there. Mayr insists that unspecialized types are less
able to emerge into new environments than specialists, and that to conclude
otherwise is a relict of typology. Archetypes could never have existed in nature.13
It is true that a combination of genetic and developmental homeostasis may give
the phenotype such uniformity and stability that it may not be able to respond phe-
notypically to a change in the environment.14 But exceptions have already been
noted, and physiological homeostasis allows the organism to go on doing the same
thing when the environment changes, and do different things when the environment
remains the same, which amount to a whole hill of phenotypic responses.
Finally, Mayr writes that the more drastic the change in environment, the more
rapid will be the evolutionary change and the more far-reaching, in general, the
structural reorganization.15 I agree with this conclusion not because of the ultimate
causal hypothesis of new, strong selection pressures, but because the emergent is
already adaptable, and to a neo-Darwinist there will be an appearance of evolutionary
change due to its sudden proliferation and diversification. Natural experimentation
has been freed from selection pressure, to diversify, and finally to be entrapped by it
again into specialization and regression. Mayr properly emphasizes the importance of
behavioral change in initiating adaptive shifts that result in changes of functional
anatomy. However, underlying the behavioral shift is the physiological adaptability
that sustains it.
Mayr also puts his finger on the kind of emergence that occurs as the result of the
coincidental integration of previously unrelated organismic features: pre-existing
building blocks, which when pieced together, give rise to an improbable new character
complex of high selective value:
The role of natural selection in these cases is apparently not the bringing-together of the
individual units; this is done by forces independent of the prospective new structure. Natural selection
enters the scene as soon as the pieces have been combined into a new complex which can
function as a unit and can respond to natural selection as a unit.16 [my emphasis, and my
inference to follow]
These independent forces would include physiological emergents arising from the
contingent co-operation of independently evolved systems, illustrated by the origin of
lactose synthetase in mammals from two proteins with previously different and
independent functions. Another example is the complementarity of osmoregulatory
pH change and respiratory hemocyanin function that allows the blue swimming crab
of Chesapeake Bay to migrate 100 kilometers in brackish water. The principle would
also apply to the coming together of previously independent symbionts.
Mayr does adduce this at the anatomical level, and tries to save it for selectionism by
giving Darwin priority. Although Darwin discussed it as serial homology and
vegetative repetition, he gave the credit to Isidore St. Hilaire (son of Geoffroy) and
Richard Owen, adding that differentiation of the parts was due to cell multiplication
acted on by natural selection.17 In The Origin of Species, Darwin also referred to Milne
Edwardss (1834) physiological division of labor, which is associated with repetitive
differentiation. If we were to be pedantic about it, we would also remember that in
Theoria generationis (1759) Caspar Wolff described the duplication and differentiation
of cells that originated as identical units in plant meristematic tissuesthereby antic-
ipating Cell Theory.
Mayr gives Severtsov (1931) and Gregory (1934) honorable mentions for dealing
with repetitive differentiation, but omits Cope and Bateson. I have already shown how
the latter duo put the concept in a non-Darwinist context. In 1929, L. J. Stadler
296 Chapter 8
discovered polyploidy and gene reduplication in barley and wheat species treated
with x rays. Severtsovs student Schmalhausen referred to chromosomal duplications
as a kind of polymerization: The most important transformations that have occurred
in various types of plants and animals are based upon an increase in the number of
similar parts and the divergent differentiation of serial homologues and
homonomes.18 Julian Huxley (1942) realized that any duplication of the
chromosomal material had evolutionary potential. Entire karyotypes could be doubled
by autopolyploidy due to mitotic error, or augmented from a foreign source as
allopolyploidy. C. W. Metz (1947) brought out the significance of duplication [and
differentiation] of chromosome parts as a factor in evolution, synthesizing current
work in fruit-fly genetics as well as Barbara McClintocks early research on corn.19
G. Ledyard Stebbins
The neo-Darwinist G. Ledyard Stebbins (1974) lists about 70 evolutionary emergences
that would fit into Lovejoys highest three categories. Then he comments that the
relative rarity of these saltatory emergencesnot that he calls them thatmakes them
less important than the much more frequent selection of minor variations that
resulted in allelic distribution changes in certain environmental conditions.
John Maynard Smith

John Maynard Smith, who is unequivocally committed to the ultra-Darwinist sect of
the Modern Synthesis, addresses similar issues in Evolutionary progress and levels of
selection (1988). He constructs a hierarchical table of levels of complexity:
l. Replicating molecules
2. Populations of molecules in compartments
3. Eukaryotic cells
4. Multicellular organisms
5. Demes, social groups
6. Species
7. Groups with cultural inheritance.20
That such assemblages exist and represent an evolutionary progression is not at issue.
Maynard Smiths crucial questions are as follows:
i. What is the nature of the genetic information that is passed from generation to generation at
each stage?
ii. How is the integrity of that information protected against selection at lower levels?
iii. How did natural selection bring about the transition from one stage to another, since at each
transition, selection for selfishness between entities at the lower level would tend to counteract
the change?21
Full and honest answers would solve some of the outstanding problems in evolution-
ary biology, but to confine the analysis to genetic information is to exclude the
organism and its actions yet again. The simple part of his third question has already
been explained. Natural selection does not bring about transitions, and the
transitions/emergences initially thrive best in the absence of natural selection.
Question two already hints that protection against selection is part of the general
answer. In a sense that selectionists find acceptable, though it is redundant to me,
natural selection participates in the stabilization of new emergent levels by fine-tuning
their connectedness. But it prevents the success of more radical natural experiments.
The integrity of information resides in the integrity of the whole organism, and the
organism is all that natural selection has to deal with. The extreme case of two
molecules or tissues or cell lineages within the same organism competing with one
another to the point of disintegration hardly enters the equation since the organism
would not survive, much less reproduce, and natural selection has no explanatory
relevance. Given a choice among similar individuals, those whose wholes are slightly
greater than the sum of their parts will outcompete those whose wholes are slightly less.
In The Major Transitions in Evolution (1995), Maynard Smith, along with Eors
Szathmry, goes further by compiling the processes involved in large-scale
emergences. However, their program is to explain the generation of emergences by
breaking down the major transitions into steps for which selective value can be
identified. Those steps may be easier for gradualists to take than high jumps to hopeful
monstrosity. On examination, however, they are revealed as smaller saltations of
unexplained origin. My own take on transitions to higher levels will be addressed in
more detail shortly, along with the outstanding problem of the generative conditions
that promote emergences, once we get out from behind the Looking Glass. I will also
respond to the units of selection problem in chapter 11. Before going on to recent
currents of emergentistic thought that lack selectionist bias, I want to re-emphasize a
cautionary note regarding oversimplifications that are made on both sides of the
mirror.
Key Innovations
While the potential for multifunctionality and adaptability is the measure of the
emergent property, evolutionary progress often seems to be realized by simple natural
experiments that produce a single crucial emergent feature. Neo-Darwinists, cladists,
and some earlier emergentists agree that specific, simple, catalytic novelties have led
to new emergent levels that enjoyed immediate high fitness and subsequent,
successful diversification. However we should be careful of seeking particulars and
ignoring the larger context. The emergent condition of flight in insects may have been
the allometric extension of dorsal flanges into discrete wings. Or was it the joints that
allowed the wings to beat with aerodynamic efficiency? Flight needed a greater
complex of generative conditions, including the arthropod exoskeleton, combined
with waterproof wax layers, and an efficient tracheal system that provided enough
298 Chapter 8
oxygen for flight metabolism. Altogether they increased insect integrity so that
everything functioned better simultaneously.
Reptiles already had multiple features that could have led to warm-bloodedness, and
some dinosaurs may have attained it. The avian lineage that perfected homeothermy
also acquired feathers, which not only insulated them but also turned forearms into
stabilizers and wings. Nevertheless, wings could only reach their avian versatility
through allometric amplification, and in association with the parabronchial
respiratory system and an increase in behavioral versatility.
Was hair the catalytic innovation for emergent proto-mammals? It insulated these
small primitive explorers during ventures into higher latitudes, mountainous heights,
or cool nocturnal foraging. However, it was only significant as one of a set of
generative conditions that included a nervous system sensitive and responsive to
temperature change, connected with shivering and non-shivering thermogenesis. Hair
not only contributed to heat preservation at the new emergent level, it also brought
epitrichal glands, whose secretions were natural hair conditioners, air conditioners,
and soft drinks for babies. And then they could diversify to produce pheromones, or
expand to become mammary glands.
In other grand emergences that have paraded in the evolutionary circus it is possible
to point to specific, inconspicuous experiments that catalyzed the main event.
Parasitic invasion, regression of defense mechanisms, where they existed, or resistance
to digestion, could be interpreted as key innovations of proto-symbionts.
Condensation of DNA and histones into chromosomes was a major innovation in
eukaryotes. Multicells needed cellular adhesion molecules. As parts of integrins that
could anchor to the intracellular skeletal matrix, and vary in their external adhesive
and receptor qualities, they were more adaptable, allowing greater differentiality in
developmental evolution. But it takes single vision to interpret these simple novelties,
however produced, as the causes of emergent transitions: e.g., Hair and feathers are
adaptations to cold weather; Wax layers are adaptations to dry environments;
Chromosomes are adaptations to chromatid confusion. It is even harder to identify
single beneficial adaptive features of cell communication and symbiosis. They add
to organismic integrity, and adaptability: the innate flexibility of constitution that
Darwin regarded as the foundation of persistence in being. And each one could only
effect the emergence in the context of the array of other functions of a whole
organism. To restructure the whole, all the other parts were required. A simplistic
search for key emergent properties could be as misleading for emergentism as selection
pressure is for selectionism.
Though rare, the ability to fly and the ability to maintain a high body temperature
are not unique to particular lineages. There have been multiple experiments in each.
Can the conditions and requirements and potentials for emergences in all the arenas
of epigenetics, physiology, behavior, associations, and environment be merged into a
single set that generates a formal universal law? For the moment, just say No. At this
point a discussion of emergentists who have come out from behind the mirror would
fit a logical sequence. However, they often emphasize emergence to new hierarchical
levels. Therefore I digress to introduce the language of hierarchies and to demonstrate
the parallels between hierarchical and emergent evolution.
Emergent Levels and Hierarchies
Molecules per se do not evolve; but their changes affect the development, physiology
and behavior of whole organisms. And some molecular changes, beyond the gene
level, are heritable. Organisms as individuals do not evolve either, but if they change,
for example by invading and responding to new environments, they can influence
evolution. To be appreciated in evolutionary terms, hierarchies need a temporal
dimension, and, in that context, organisms do contribute to the evolution of their
lineages through development, physiology, behavior, and association.
Maynard Smiths tabulation of levels of selection demonstrates how, when we
come out from behind the Looking Glass, we must deal with hierarchical emergent
levels, albeit with natural selection relegated to a stabilizing rather than an innovative
role. One thing to keep in mind from the beginning is that emergence to higher levels
does not always involve the addition of a new layer on top of the older ones. In the
case of the vertebrate neocortex and the expansion of the cerebral hemispheres it does
appear that way superficially, but they are functionally internested with foundational
systems, such as the limbic and hypothalamic portions of the older brain, and its
ancient medulla that regulates some important functions of homeostasis.
In the prologue to emergence in chapter 2, I noted how similarly Henry Drummond
(1894), Samuel Alexander (1920) and John Holland (1998) expressed how the new
emergent level has a new relatedness whose qualities allow it to perform innovatively,
without disobeying the laws that constrain the lower levels. Alfred North Whiteheads
Theory of Organic Mechanism, set out in Science and the Modern World (1925),
illustrated this concept with an example that I here expand. He said that the behavior
of an electron in a nerve axon is unlike that of a free electron in a disorganized,
non-living system, because it is subordinate to myelin insulation, the passage of
the electrical impulses in the nerve, and the physical restraints of the axon. His point
is well taken, though we should be looking at ions rather than electrons. Nerve
impulses are made possible by the electrolyte composition of the intracellular and
extracellular environment, which is governed by biological ion pumps and gated
channels switched on and off by neurotransmitter molecules. Initiation of an
autonomic nerve impulse can be stimulated by the local environment, and then
overridden by the central nervous system. For example, secretion of the various
hormones and enzymes of the upper alimentary tract, which are initially under neural
300 Chapter 8
stimulation, may be terminated by somatostatin, the body stopper hormone, in

response to an emergency that requires that blood be diverted from the intestinal
mucosa.
In the language of hierarchy theory, at the focal level of the nerve cell (the level
under scrutiny), an electrical potential can be built up according to physicochemical,
and biological conditions. At the lower, generative level, there exist operational
constraints imposed by the availability of chemical energy, the state of membrane
pumps and channels, and condition of receptors for neurotransmitters. The neurons
action is triggered or inhibited by the influence of a higher constraining or organizing
level. Behavioral and cognitive levels can activate or override the lower levels. To flee
or hide from a predator is a common automatic reflex in lower animals. But in higher
animals, intelligence can overrule automatic reactions and suggest different
behavioral options, such as pausing to check for fire below, before leaping out of frying
pans. Logic and language impose yet another regulatory levelthe challenge Friend
or Foe? can determine the degree of danger of the unknown and suggest options
before anyone gets shot. At no point has the physical nature of the electron or ion
been compromised, nor the physicochemical action of the nerve cell, nor the local
hormonal and vascular qualities of an organ system, nor the automatic or reflex
functions of the nervous system. Each of these represents a hierarchical level with its
own array of holons and distinctive emergent features.
The intrinsic emergent evolution of self-organization involves hierarchical relation-
ships between building blocks that include molecules, genes, tissues, and organs.
Organisms are also members of intraspecific and interspecific hierarchies, whose
organization may wax and wane with environmental change. There are two kinds of
biological hierarchies: control hierarchies and compositional hierarchies. Here I
am taking a leaf from Stanley Salthes Evolving Hierarchical Systems (1985). The chain
of command in a nervous system exemplifies a control hierarchy. Conscious choice
orders the central nervous system to activate muscles and produce behavior. Some of
the neural control hierarchy, as well as the hormonal system, is involuntary. Although
we have seen how it can be affected by the larger environment, including other
organisms, the intraorganismal control hierarchy is a very distinctly independent unit.
A compositional hierarchy can depict the biosphere as the largest component (or
even include the entire planet or the entire cosmos). Within it are internested
biocenoses, ecosystems, communities, populations, demes, organisms, organs, cells,
molecules. The compositional hierarchy is usually depicted with a Venn diagram of
circles within circles. (By the way, the figure that I have used for the three-ring circus
within the big top borrows in part from a Venn diagram but owes nearly as much to
electron-orbital depictions and the Celtic triskelion. In other words the image is a pic-
tographic simile, not a formal attempt at marrying causality, function, and structure.)
Causal arenas could conceivably be forced into a Venn diagram, and thereby be made
more convincing to hierarchy theorists. I will demonstrate how misleading such

simplicity can be. But for the moment I return to the nuts and bolts of hierarchical
systems.
Holon is a useful general term for the units that are usually associated into co-
operative groups arranged in a hierarchical order of interaction. From the
physiologists point of view an array of molecular holons, such as hormones and
enzymes, may be characteristic of an organ-level holon like the pancreas or liver. Such
organs are under the regulative control of higher-ranking holon organs,. such as the
pituitary and the brain. The word holon was used by Arthur Koestler in The Ghost in
the Machine (1967), building on the foundational ideas of J. H. Simons 1962 article
The architecture of complexity. For Koestler, holon meant simply a subunit or
module of a hierarchical level, which is the most effective usage. A holon could be part
of a hierarchical anatomical structure, i.e., part of a compositional hierarchy, and part
of a control structure, i.e., under the command of a higher level as well as interacting
with other holons at the same level. In more recent literature, the treatment of this
subject comes under the heading of modularity, where holons are called modules.
Furthermore, repetitive differentiation would be taken as a subset of modularity. I
prefer holon because of its holistic implication, but I will use holon and module
synonymously. Waddingtons (1966) version of modularity did little to advance the
principle. The repetitive differentiation component of modularity was brought to the
fore in Susumo Ohnos Evolution by Gene Duplication (1970). Rupert Riedl works the
repetitive differentiation of modules into the organization of hierarchical patterns, in
Order in Living Organisms (1978). Although he emphases its morphological aspects, his
general principles apply at all hierarchical levels. Developmental evolutionists such as
Rudolf Raff (1996) and Scott Gilbert (1997) have popularized modularity, and
Modularity, edited by Werner Callebaut and Diego Raskin-Gutman (2005) is the latest
and most comprehensive work.
Koestlers illustration of the hierarchical structure of an army emphasizes the chain
of command. Individual soldiers are holons ranked into higher holonsplatoons,
under a junior officer. Companies are holons that unite several platoons under a more
senior officer, and so on up through regiments and brigades. Thus, any rank, or level
of organization, consists of a number of separate but coordinated holons, each of
which have a self-assertive tendency and an integrative tendency; in other words,
independence and cooperation. An array of holons may be identical, as in the case of
multiplied genes that turn out large amounts of a given protein. Simple duplication of
modules evolves first, and may immediately serve the function of increasing a crucial
process. With or without such a function an array may then differentiate. An example
would be the ensemble of genes for enzymes with identical functions but different
temperature optima. These are what W. R. Ashby (1952) called step mechanisms.
They are usually turned off until appropriate conditions for their operation arise. An
302 Chapter 8
array produced by repetitive differentiation may alternatively form a biochemical

pathway, taking a substrate through several changes until the final product appears.
Its organization may be made more complex by branching, the final route being
decided by prevailing physicochemical conditions.
Holons, or modules, at the anatomical level evolve according to similar principles,
first multiplying and then differentiating. If the holon begins as a multifunctional
organ, the repeated units may specialize for particular functions, involving both
anatomy and the organization of biochemical syntheses. The progressive evolution of
the gill pouches of primitive vertebrates illustrates how far such physiological special-
izations can diverge. Just as independent biochemical pathways might contingently
associate, so also do formerly independent anatomical units cooperate by progressive
packaging. The close physical association of the pituitary gland with the hypothala-
mus, via a vascular portal system, is an example.
The evolution of higher levels of organization is what emergence theory is largely
about, so when they first appear it is appropriate to call them new emergent levels.
Recall that the level of organization or emergence under consideration is the focal
level, and the level below it is the generative level. I have already hinted at the
importance of holistic analysis of the generative conditions for a given focal level, in
assessing how emergence to a new level occurs. David Rollo, whom I regard as an
honorary emergentist, comments on how hierarchical structure is apposite to
emergence:
Hierarchical organization may be crucial for compartmentalizing interactions and allowing large,
complex systems to retain stability. Not only does hierarchical organization provide reliability
and stability but modularized structure also allows modification of subcomponents without
global disruption. Thus, hierarchical structure allows systems of great complexity, which also
retain the ability to evolve. Both are key attributes of life.22
Now what do my other fellow biological emergentists have to say about hierarchies?
Order in Living Organisms (1978) merits Rupert Riedls conscription as an emergentist.
For example, Riedl refers to quick breakthroughs to new forms of organization.23 He
frequently alludes to how the reorganization of modules brings new adaptabilities that
are then lost as a result of canalization. And, in his conclusion he notes that the
highest states of order involve the greatest possible differentiation, complexity, and
individualization.24
Regarding hierarchies, Riedl writes:
Hierarchical order is characterized by features (or concepts) whose fields of validity do not
overlap but are contained within each other, so that several lower concepts of equal rank are
usually included in a higher concept. The higher concept specifies the significance of its lower
concepts, and the latter specify its contents.25
Since the evolution of hierarchies depends on the definitive fixation of additional

features, repetitive differentiation is important.26 Riedls synthesis is thoroughly
Aristotelian, marrying a hierarchical systems degree of complexity with its degree
of integration. The former is defined as no more than the sum of holons. The latter
depends, first, on the degree of coordination. Some systems might operate
effectively if its holons vary a little, but not if they vary a lot; i.e., there is some limit
of tolerance to variation. Integration also works according to a degree of
dependence. That refers to how essential a particular holon might be in a dynamic
system. Riedls example is an automobile that can be driven indefinitely without a hub
cap, but not with a bent axle.27 He places strong emphasis on the importance of hier-
archical position in determining how much of the rest of the system will be adversely
affected if it changes.28 Numerous biological examples are provided of dramatic
phenotypic variations that arise late in the epigenesis of orchids, insects, birds, and
antelopes when Riedl discusses systems of maximal freedom from genetic
determinism.29 But he also points to organs that have been strongly conserved
throughout evolutionary history due to their epigenetic burden, presumably
because they have key hierarchical positions, and their alteration would be disintegra-
tive. William Wimsatt (1986) calls this generative entrenchment. Epigenetic burden
can be referred back to the accommodation problem of evolutionary developmental
change, which worried Bateson, and made Fisher reject the hopeful monster. Yet, late
phenotypic developments or not, Riedl is showcasing not only hopeful, but successful
monsters. And some modern theorists, Riedls students among them, have done an
end run around the accommodation difficulty, as I will point out in the next chapter.
For the time being it is sufficient to acknowledge that hierarchical position is indeed
important, but that there need be no adverse consequences arising from early
deviation if there is harmonious reintegration during the chronological processes of
epigenesis.
Riedl was the first biologist to provide a comprehensive theoretical analysis of the
evolution of hierarchical organization, and an inspiration to those who were to follow,
including myself. Also among them are Elisabeth Vrba and Niles Eldredge (1984):
Hierarchy is a central phenomenon of life. Yet it does not feature as such in traditional biological
theory. The genealogical hierarchy is a nested organization of entities at ascending levels. There
are phenomena common to all levels: (1) Entities such as genomic constituents, organisms,
demes, and species are individuals. (2) They have aggregate characters. . .but also emergent
characters (arising from organization among subparts). Character variation changes by (3) intro-
duction of novelty and (4) sorting by differential birth and death. Causation of introduction and
sorting of variation at each level may be (5) upward from lower levels, (6) downward from higher
levels, or (7) lodged at the focal level. The term selection applies to only one of the possible
processes which cause sorting at a focal level. Neo-Darwinian explanations are too narrow, both
in the levels (of genotypes and phenotypes) and in the directive process (selection) which are
304 Chapter 8
stressed. The acknowledgement of additional, hierarchical phenomena does not usually extend
beyond lip service. We urge that interlevel causation should feature centrally in explanatory
hypotheses of evolution. For instance, a ready explanation for divergence is selection of random
mutants. But upward causation from genome dynamics (or downward causation from the hier-
archical organism) to the directed introduction of mutants may be more important in a given
case. . . . A general theory of biology is a theory of hierarchical levelshow they arise and
interact.30
If that were so, an emergence theory would be little more than a theory of hierarchi-
cal levels. How they arise would certainly be the crucial question, and how they
interact its elaboration. Sorting would be seen as the consequence of the quality of
novelties as they emerged, not as an explanation of their generation. And sometimes
it is a barrier to evolutionary progress. Moreover, throwing demes and species and
genes into the pot distracts us from the organism, and its immediate interplay with its
environment. Vrba and Eldredge do not come out and say it in so many words, but
you dont have to read too deeply between the lines to see that a general theory of
biology would have to rest on a new theory of evolution.
In What are the biotic hierarchies of integration and linkage? (1989), Vrba calls
for an expanded evolutionary theory and baldly states that it is dishonest to claim
that that the Modern Synthesis can be stretched and modified to infinity. At this point
I have no wish to engage in semantic quibbling, but should explain that she uses the
word structure in the special sense of a biological emergent phenomenon.
Structuralists would use the expression dynamic structure which includes develop-
mental, and physiological functions, as well as anatomy. The generative conditions at
any hierarchical level is usually based on some kind of structuremolecule, cell, organ
etc. Although Vrba knows that behavior has a downward causal effect on both
physiology and anatomical development it stretches the word structure to include
behavior, the physiogenic interpenetration of organism and environment, and the
interaction between the organism with its own kind, or other organisms in its
environment. Although simplistic hierarchal analyses tend to be empty of such inter-
actions and interpenetrations, Vrba does not omit them. Therefore, as I quote from her
essay I will substitute (in brackets) emergent for structural and emergence for
introduction of structure. Aggregate characters will be left alone as the additive
parts that do not result in greater wholes:
Introduction (or origin) of new variants. De novo introduction of both aggregate and [emergent]
characters occurs at all levels. I use the term introduction in the simple vernacular sense of a
first appearance to refer solely to the first origin of a new variant, in distinction to sorting
among variants. Thus, [emergences] at the gene level included various forms of gene mutation.
[Emergences] at the organismal level refers to the first appearances of phenotypic mutants,
including minor phenotypic innovations and the one-step origins of complex ontogenetic products
that may diverge considerably from the parental phenotype. At higher levels heritable [emergences]
occur less frequently than at lower and require changes at all lower levels.31
The emphasis in the second last sentence is mine. Hopeful monsters, whatever they
are called, deserve the attention.
Vrbas rules of emergence that apply in common to the evolution of all levels
follow, with some comments of my own at the end of each in brackets.
1. Each new hierarchical step was initiated by the origin of recognition and interaction
among entities already present and differentiated at the existing level. Thus,
recognition between cells was required for the origin of sex (i.e. species sensu stricto)
and of metazoan differentiation, just as it still is during each reproductive process and
each ontogeny. [Being in the same place at the same time: I think this rule justifies my
lumping of associative emergences in chapter 3.]
2. Complex structures and processes at existing levels presented a pool of available

materials and, at the same time, strong constraints for integration in the new
evolution of higher levels. Since then, in evolution within each level, the same
principles have applied again and again. [Repetitive differentiationseparation of
offices and concurrence of efforts.]
3. During the earliest evolution of each higher level, as emergent structure and
therefore selection were initiated, there must have been selection wars between
higher and lower selection regimes (Buss 1987, and below). These wars were concluded
long ago in net favor of the higher individuals that exist. (Where the higher level lost,
it is not there for us to see.) [Some experiments in the separation of offices are simply
disintegrative, and dont need to be explained in metaphorical militaristic terms.]
4. Sorting and change at lower levels need not affect a higher level in more than a
sums-of-parts or aggregate way (such as cellular dynamics within the same organism,
and organismal turnover and change within persisting species). Yet any selection at
higher levels must entail sorting among individuals at all lower levels. [Co-adapta-
tional fine-tuning follows the emergence of physiological novelty, but does not
generate further emergences. However, fine-tuning that gives the organism a slight
edge will likely result in differential reproduction among organisms that share the
emergent property.]
5. A related observation is that hierarchical evolution has involved a progressive loss

of autonomy at lower levels as autonomy increased at higher levels.32 [For example, we
dont regenerate as well as earthworms when we are cut in twoimperfection of
adaptation?]
Much of what I have developed in earlier chapters integrates with Vrbas assessment
of the relationship between hierarchies and emergence. At this stage of development
306 Chapter 8
of an emergence synthesis we need rules that apply at all levels, within levels and
between levels. Otherwise we will never reduce to a model that is easier to grasp than
the confusing reality. Yet, in addition to rules common to all hierarchical levels, we
still must find newly emergent rules that are not to be found at lower levels.
Coeval with Vrbas thoughts on the importance of hierarchical evolution are those
expressed by Stanley Salthe in Evolving Hierarchical Systems (1985). He too strays from
his neo-Darwinist roots, treats Koestlers ideas with some respect, and recognizes the
relationship between hierarchical evolution and emergence. For example, he observes
that the predictability of emergence is low where there are many possible generative
conditions. But when they are few and repetitive, the resulting emergences are obvious
and predictable. Therefore there is a degree of observer bias.33 Salthe also accepts that
differentiation produces more complex new holons whose interactions provide new
generative conditions. And, he notes, the organic evolutionary process obviously is
easily registered in the organism, contemplation of which was the original impetus to
imagine that process. Traditionally, organic evolution is measured and tabulated by
organismic alterations in time.34 This traditional measurement also applies strongly
to emergent evolution. But Salthe then extends the assessment to population and
ecosystem levels. How he does it makes good sense to me, since it involves interactions
within communities and between demes that have a downward causal effect on their
constituent organisms. But he runs the risk of pandering to population thinking as
a superior approach to the measurement of evolutionwhich brings me back to the
oversimplification that can come from the compositional hierarchical concept. It is
often used as a filing system for entities based upon their degree of magnitude. For
example the cosmos contains biospheres, made up of ecosystems, communities,
demes, and organisms. Then the organisms contain organs, cells, and molecules.
However, emergent levels cannot easily be equated with compositional hierarchical
levels. Within the organism, the evolution of the two have identifiable similarities. For
example, this hierarchical systemmolecular systems < simple cells < complex cells <
simple multicells < multicells with differentiation and integration < complex
organismsis equivalent to a series of emergences. Moreover, it is recapitulated in part
during the epigenesis of the individual organism. However, emergences, and new rules
that they generate, have not obeyed this kind of simple progression. At many times in
evolutionary history the activity of the higher levels has had a downward directional
effect on the lower levels. Emergent adaptability may come at the molecular level long
after emergent complexity has been completed at the gross anatomical level.
Furthermore, the compositional hierarchical system that has just been laid out is often
continued as organism < deme < population < species. In a Venn diagram these are just
circles within circles; but in reality there is a major break between the organism and
its environment, physically, biologically, and philosophically. Demes and populations
are entities, but they are not higher, regulatory, emergent novelties. They always
existed, regardless of the emergent level that had been reached, whether it was a group
of simple proto-cells, or a gaggle of geese.
To be sure, the coordinated behavior of a flock of birds is an emergent phenomenon.
And social behavior has a feedback effect on the physiological state of the individuals
that make up the group. But emergent evolution does not continue on a larger scale
into demes and populations. There is a break point. We know how important families
and societies are for the intellectual development of young humans. But in most other
organisms there is a gulf in evolutionary causation between intraorganismal and
interorganismal phenomena. Such caveats regarding the comparison between
emergent evolution and the evolution of hierarchal systems were behind my original
decision to organize my thoughts in the context of causal arenas. Ultimately, however,
the latter also need to be analyzed in terms of the former.
Recent Currents of Emergentistic Thought
In the early 1970s, when I first read C. L. Morgan and began to take an interest in evo-
lutionary emergence, a movement called biological structuralism was developing. It
addressed the hierarchy of biological organization, and the emergence of higher levels
of from simpler ones. Structuralism gives a limited interpretation of emergent
evolution, since it largely ignores the significance of environmental contingencies,
including the potential for organismal associations. The structuralistic concept of
autoevolution developed by Lima-de-Faria (1988) hints at emergence, in the loose
sense of the appearance of a new phenomenon, but for him everything new is old
again: innovations primarily arise from the ancient physicochemical nature of the
universe. The significance of physical autocomplexification cannot be gainsaid when
the origin of life is being considered. But subsequent emergences in biological
evolution have largely been generated by biological causes.
Neil Campbells popular introductory textbook Biology presents hierarchy of organ-
ization as the first topic of the first chapter, with emergent properties close on its
heels:
With each step upward in the hierarchy of biological order, novel properties emerge that were
not present at the simpler levels of organization. These emergent properties result from interac-
tions between components. A molecule such as a protein has attributes not exhibited by many
of its component atoms, and a cell is certainly much more than a bag of molecules. . . .35
Campbell goes on to explain that it is unnecessary to adduce vitalism to explain

emergence, and then points out that DNA function was far better understood once its
interactions with other cellular functions were discovered. In other words, a holistic
approach was necessary: Biology balances the pragmatic reductionist strategy with
the longer-range objective of understanding how the parts of cells and organisms are
functionally integrated.36
308 Chapter 8
That would be fine if it were true. Fifty years ago, when DNA structure was
elucidated, a few wilderness voices cried about the need to understand the control of
gene expression. Jakob von Uexkll had foreseen the need for a hierarchical genetic
regulatory system as soon as the first results from Drosophila research began to be
published. L. L. Whyte (1949) had already anticipated the importance of the organi-
zation of interacting genes and enzymes, admonishing reductionistic biologists for
thinking of the cell as a bag of molecules. In 1957, C. H. Waddingtons The Strategy
of the Genes included not only the adaptational significance of their mutations, but
epigenetic variation of their expression and integration. What took the rest of us so
long? And when it comes to working the concept of emergence into evolutionary
theory as well as physiological organizationwell, that is why you and I need to have
this tte--tte.
In Lifes irreducible structure (1968), Michael Polanyi wrote about how emergent
levels in hierarchies imposed boundary conditions on the lower levels. He had already
remarked in Personal Knowledge (1958) that it was difficult to get such ideas accepted
unless the recipients are willing to learn new words and definitions. If they have a
premonitory distrust or fear of what might be in store they will resist the neologisms
and the framework of the ideas. Proponents of a new system can convince their
audience only by first winning their intellectual sympathy for a doctrine they have
not yet grasped.37 It may not now be as insurmountable as Polanyi suggested, due to
a slow, subconscious osmosis of the emergent property, holons, modularity, and
hierarchiesto the point where emergence is commonplace in the titles of
current books.
The neurobiologist Roger Sperry was an important latter-day emergentist, particu-
larly interested in research into split-brain phenomena and the role of the corpus
callosum in the integrity of mind. I have already mentioned his emergentist epiphany
in the 1960s. Although he concentrated largely on mind as emergence, Sperry
continued to have a significant, if controversial role, in promulgating an emergent
interactionism that merges with views that Susan Oyama has elegantly expressed.
My own tentative ideas on the need to develop a theory of emergent evolution were
published in Evolutionary Theory: The Unfinished Synthesis (1985). They are re-dissemi-
nated throughout the present work, so I mention them only to map my own entry
point on the road to emergentism. Eugene Balon was also developing emergentistic
ideas before his publication of a tentative theory of saltatory ontogeny in 1986. Its
major premise is that a series of stable developmental phases is punctuated by
thresholds, at which bifurcations of behavior, physiology and anatomy with evolu-
tionary potential are possible. This intuitively leads to the notion that saltatory
ontogeny recapitulates saltatory phylogeny, which I would call phylogenetic
emergence. We agree that ontogeny is not predetermined by a genetic template, but
that the two are in a state of dynamic interaction. The following authors merit their
own sections for their recent contributions to emergentist thought.
Gerd Mller and Gnter Wagner

Gerd Mller and Gnter Wagner discuss emergentism in all but name in their 1991
essay Novelty in evolution: restructuring the concept. They begin by pointing out
that the problem of the origin of novelty was acknowledged by Darwin as well as by
his critics. But advances in genetics provided only the general answer of mutational
change, and the problem was subordinated to the species question and dissipated by
adaptationism. They acknowledge that Ernst Mayrs hypothesis of function change, in
terms of repetitive differentiation of structure, is part of the picture. But a major
unanswered question is Can new structures arise without a change of function?38
Taking the level-of-organization approach, they attend first to populations,
ecosystems and natural selection. Giving these short shrift, they go down to the gene
level. Here they acknowledge the evolutionary significance of structural and
regulatory gene mutations, chromosome mutations and polyploidy, noting that none
of these dominate as candidates for the emergence of novelty. But for the most part
their focal level is morphogenesis. Here I will abstract their broader evolutionary gen-
eralizations, returning to the details of developmental heterochrony in the following
chapter.
Mller and Wagner are primarily concerned with any morphological novelty that
can be defined as a structure that is neither homologous to any structure in the
ancestral species nor homonomous to any other structure of the same organism.39
They recognize that the appearance of novelties derived by differentiation from
repeated elements is important, as are innovations derived by regression. But they
concentrate on Lovejoys primary category of new events irreducibly different from
old ones. In placental mammals, the novel corpus callosum in the forebrain cross-
connects the expanded cerebral hemispheres. Unique marsupial bones emerged in the
mammals, and in marsupials they support the pouch, but placental mammals have
lost them. Epitrichal sebaceous glands that gave rise to sweat and mammary glands are
regarded as true novelties. Innovations at lower taxonomic levels include the thumb
of the giant panda, and horns and antlers in hoofed mammals.
I take issue with the assertion that non-trivial novelties, including those that arise
by differentiation of repeated elements, and truly novel elements such as new bones
or fiber tracts must have profound adaptive value, and hence can be fixed in
populations by natural selection.40 For one thing, nontrivial and profound
amount to the same thingselectionist redundancy. For another, if they emerged
suddenly as full-blown adaptive features, the process was likely saltatory. And for a
third, they could first have emerged as trivial features beneath the attention of natural
selection. But the more important questions about morphogenic emergences proposed
by Mller and Wagner deserve serious attention:
1. What is the generative potential of the developmental mechanisms to the members

of the ancestral taxon?
310 Chapter 8
2. What are the critical changes in generative mechanisms of development that

allowed the realization of the derived feature, i.e., the novelty?
3. Which genetic changes were the reason for the heritability of morphological
novelties?41
These can largely be analyzed by comparative studies of extant organisms, even

although the direct ancestors of emergents with novel properties are extinct. However,
Mller and Wagner caution us that the organismal-developmental context needs to be
known before question three can be answered. To initiate a study of the generative
modes of morphological emergence, they organize them into the following categories
whose contents I paraphrase, again with my personal comments in brackets.
Hierarchical Organization
Levels of organization from molecules to ecosystems are hierarchically ordered. In
development hierarchical organization is built in a chronological sequence. Therefore
[as Geoffroy long ago realized] changes in early stages effect large changes in later
stages. Since concrete examples can be provided of the effects of early changes in cell
lineage, this is no longer a merely speculative supposition.
Interactivity and Dissociability

During development lineages that diverge from one another can still form a network
of interaction. [These can settle into the dynamic stability of homeorhesis, as
Waddington called it. Or, as Wimsatt (1986) would say, the degree of interaction
determines the degree of generative entrenchment.] Thus, development is canalized
[systems are entrenched], and change requires dissociation of networks. Nontrivial
novelties emerge despite epigenetic constraints that prevailed at the generative level,
i.e., in the ancestors.
Equilibria and Thresholds

Existing conditions of homeorhesis are most vulnerable to change at critical stages or
thresholds in development. There is therefore a potential for saltatory, emergent
novelty if physicochemical influences are altered, or heterochrony occurs. [Like
Lovejoy (1927), Mller and Wagner allow that their categories of the generative modes
of emergence are not mutually exclusive. Also, they seem to view emergent novelty in
the context of Spinozan/Darwinian persistence in beingno criticism implied.]
The origin of new body plans required the origin of morphological novelties, but it
also requires the integration of this new character with the other parts of the
organism. In this context it is irrelevant whether integration is due to functional
necessities or due to epigenetic interdependencies. What counts is that some
characters acquire an indispensable biological role that is conserved in spite of

changing adaptive pressures.42
Brian Goodwin and Ricard Sol

I have frequently referred to Brian Goodwins publications that deal with emergent
phenomena. With its call for a Science of Qualities, How the Leopard Changed Its Spots
(1994) influenced my own thoughts on the matter. Such a science would emphasize
the generation of change and the nature of novelty. During the development of the
present work, he and Ricard Sol published Signs of Life (2000). They offer a selection
of physicochemical and biological emergences whose properties can be mathemati-
cally captured, but which, as non-linear dynamic processes, are unpredictable. This
approach complements that taken by John Holland, and together the two books
contribute to a solid quantitative foundation for emergentism.
Jack Cohen and Ian Stewart

Jack Cohen and Ian Stewart, in The Collapse of Chaos (1994), come close to a formal
description of emergence when they say that a collection of interacting components
can spontaneously develop collective properties that seem not to be implied in any
way in the individual pieces.43 Emergences collapse chaos in the sense that they bring
order to chaotic confusion. Cohen and Stewart also accept the importance of both
intrinsic and extrinsic events. Like Stuart Kauffman, and Ivan Schmalhausen before
him, they see intrinsic events as responses to a sort of internal emergence pressure, an
inherent tendency of simple systems to complexify themselves, but beyond which
there are processes in which totally different rules converge to produce similar
features, and so exhibit large-scale structural patterns. These events depend on the
extrinsic contingencies of other independent systems, occurring where the
interaction of several spaces of the possible leads to an explosion of the combined
space and the emergence of features that cant in any sense be traced back to the
components.44
Cohens and Stewarts enthusiasm is encouraging, and their broad analysis is on the
right track. But before these hunches are followed, more exhaustive legwork is
required, and it will find no support for the mutual exclusivity of the intrinsic and
extrinsic. The same is true of Kauffmans quest, although he does not use the word
emergence formally, associating it with the evolution of self-organization.
Stuart Kauffman
Since The Origins of Order: Self Organization and Selection in Evolution (1993) gets close
to a theory of emergence, I am obliged to compare what Kauffman has said with my
own opinion. Although he is not quite out from behind the Looking Glass, Kauffman
ventures that we must integrate the fact that selection is not the sole source of order
312 Chapter 8
in organisms. Then he acknowledges that biologists are secretly aware that selection
must be working on systems which to one degree or another exhibit order by
themselves. DArcy Thompson (1942) told us so with eloquence years ago, but we have
not troubled to think through the implications. How strange, yet therefore how
inviting, that we may one day bring ourselves to see life in a new light.45 Coming
closer to the heart of the matter, Kauffman adds:
We shall in fact find critical limits to the power of selection. As the entities under selection
become progressively more complex, selection becomes less able to avoid the typical features of
those systems. Consequently, should such complex systems exhibit spontaneous order, that order
can shine through not because of selection, but despite it. Some of the order in organisms may
reflect not selections success, but its failure.46
Kauffman quests for rules of autonomous self-complexification that ought to shine

with grail-light through the murk. But a rule that can be derived for one level of
emergence may not offer predictions for emergence to the next level up. An
explanation of the origin of life might be surprisingly easyan expected emergent
collective property of a modestly complex mixture of catalytic polymers, such as
proteins or catalytic RNA.47 What is unsurprisingly easy about this assessment is that
it depends on a priori knowledge of the existence of life and its qualities. Can such an
emergence be post-predicted: inferred from a knowledge of the generative level of
organic molecules?
John Holland
Holland deals largely with emergent order in very simple non-living systems whose
structures and functions can be described with total mathematical rigor. But his
models and metaphors touch on biological systems sufficiently to allow our ideas to
interdigitate. Therefore I prefer to introduce some of his terminology rather than to
paraphrase him in the vernacular.48 He begins with a set of elements and defined laws
that govern their combination, taking the model of a board game involving pieces
that respond to the stimulus of the play according to the constraints of space and
permissible action. Thus, he has a set of generators functioning according to if [such
be so] then [do this] clauses or stimulus-response actionsin other words, reactions to
simple algorithms or guiding programs. The state of the system is equivalent to the
disposition of the game pieces on the board at any one time, or the various conditions
of neurons in a neural network.
The transition function brings in the effect of an input or stimulus on the state of
the system that results in a new state. As the system changes state, different strategies
can come into play, if it is possible to respond in more than one way, and if the
responses are recursive, i.e., can be evaluated before being put into action. The use of
strategy delineates a trajectory or unique sequence of states as the game progresses.
This is relevant to orthoevolution, regardless of its causal interpretation. The path of
the trajectory is also contingent on the variety of stimuli presentedthe opponents

moves, in the example of a board game. These are not very predictable if there is a
wide choice of options.
General concepts that appear as Holland builds his arguments include building
blocks, or repeatable features that appear in systems with emergent properties. They
are equivalent to holons or modules. They and the systems that they combine to form
can be modeled by particularizing their salient features and the rules that they obey.
Agents are holons that interact in the system, like billiard balls on a table at the
physical level. Cells in a multicellular organism, or organisms in a social system are
agents. The final neologism necessary for interpreting Holland is the constrained
generating procedurea system that combines the elements, rules and interactions
that are capable of producing emergent novelty.49 Building upon these generalizations,
Holland produces the following aphorisms. After each, I paraphrase his explanation
and examples, together with my own comments and examples, in brackets.
1. Emergence occurs in systems that are generated.
Emergences arise in systems composed of a finite array of multiple similar holons

whose interaction changes their state. In the model system of a board game like chess
the pieces have been manufactured as several sets of identical chessmen. [Similarly, in
a cell there are various kinds of proteins, often existing as multiple copies. What is
important here is change in state over time due to the operation of transition
functions.]
2. The whole is more than the sum of the parts in these generated systems.
[I have illustrated how this can be so by the simple example of symbionts that can
turn detrimental properties into usable ones, or negative into positive.] Holland says
that the overall behavior of the generated system cannot be predicted by knowing
how the parts can behave: The definition of the generated system, though it
determines all the rest, is no more than a simply described starting point; subsequent
activities can be determined only by extended examination and experiment. In this
sense, more comes out than was put in.50 Thus, a game like chess, played and studied
for many centuries, continues to produce surprises.
3. Emergent phenomena in generated systems are, typically, persistent patterns with

changing components.
A physical illustration is the standing wave that persists in front of a rock in a swift
stream, although the water molecules are constantly being replaced by new ones all
314 Chapter 8
the time. [Similarly, methylation and binding patterns that are initially induced by the
environment can persist from one generation to the next. The most general biological
example of a persistent pattern is the organism, whose molecular makeup turns over
continuously. The pattern of the organism persists to a large extent in its offspring.]
4. The context in which a persistent emergent pattern is embedded determines its

function.
[This relates to organismal multifunctionality as well as to its environment. The

persistent pattern of gill arch bones, for example, is used in different ways in a chrono-
logical evolutionary sequence: gill function; jaw function; ear function. This is a very
productive model that I have touched upon in the physiological arena and will come
back to in the next chapter.]
5. Interactions between persistent patterns add constraints and checks that provide
increasing competence as the number of such patterns increases.
[The constraints and checks in developmental canalization, for example, do make the
developing embryo more competent at maturing true to type. This is an obstacle to
evolutionary emergence.] But there is a saving qualification: the possible sophistica-
tion of response rises extremely rapidly (factorially) with the number of
interactants.51
6. Persistent patterns often satisfy macrolaws.
For example, predicting how an animal with a stereotyped behavior pattern will
respond to a stimulus does not require recourse to microlaws such as the physics and
chemistry of vision and chemoreception. [Nor are the persistent patterns of homology
determined by genetic microlaws.]
7. Differential persistence is a typical consequence of the laws that generate emergent

phenomena.
[Amen to consequences coming after generative causes. Such persistence could be

due to adaptability, and it is not smuggled in from high order biological systems, but
is found in a simple computerized checkers-playing program that can alter its strategy
by re-evaluation in terms of previously successful actions.] Holland also writes:
Generalists are much better tested for persistence than specialists, because the
generalists receive many trials in a wide range of situations, in the same time that the
specialists receive just a few trials. As a result, the generalists supply a firm niche for
the specialist that can interact with them.52 [He overlooks the fact that generalists
possess the qualities for persistence before they are tested. However, his point does
bring out the significance of emergences involving symbiosis and ecological associa-
tions as well as the self-sufficient emergent property of adaptability.]
8. Higher-level generating procedures can result from enhanced persistence.
Here Holland specifies symbiosis as a generator of enhanced persistence, commenting

that it yields patterns extremely unlikely on an a priori inspection of the original
generator[s]. [This statement can also be usefully reversed to infer that adaptability is
a generating condition for higher-level emergences. This applies to major adaptational
changes as well. The persistent striving of the hippopotamoid ancestor of whales to
swim out of its depth preceded the genetic assimilation of more whale-like anatomical
phenotypic changes. But this all depended on its adaptable placental physiology.]
My major criticism of Hollands reductive rules is that some of them intuitively

smuggle contraband from higher-order systems. This dilutes the mathematical rigor
that he demands of emergentism and tries to provide for his simplest models. In
taking the high road I have not bound myself by such constraints. I can smuggle and
dilutei.e. write about downward causation and interactionto my hearts content.
Life is not a board game with finite rules that are changed by mutual agreement of the
players. Instead, stable dynamic systems are disequilibrated into partial chaos by
entities that break the rules. Physicochemical and biological contingencies inexorably
impose new conditions. But it is more important that as emergent evolution progresses,
it allows greater freedom of action for the organism, which has a feedback effect on its phys-
iological makeup and morphogenesis. Holland does not exclude extrinsic effects, but
underestimates them.
It is alluring to draw parallels between the emergence of ideas from game playing,
or any cognitive emergent process, and the emergence of biological innovations. But
rigor is lost in the gaps between metaphor and actuality. Nevertheless, if Hollands low
road does not quite arrive at evolutionary emergence, it reaches, as he says, a way
station for the expedition, where I can compare notes with him. Such an exercise
shows us how the generative conditions for emergence include systems with multiple
components that can be differentiated, and thereby become more adaptable.
Emergence produces new macrolawsthey reflect the degree to which the whole is
greater than the sum of its parts. And the further emergent evolution progresses the
more it is likely to occur. These inferences have been frequently drawn by emergen-
tists, and others I have conscripted. And when show me comes to prove it,
Holland has the edge.
316 Chapter 8
William Wimsatt
The philosopher William Wimsatt, who has been writing about the meaning of
complexity and organization for a quarter-century, has recently paid more attention
to emergence, by using systems reduction (or simple systems analysis). The success
of this approach is illustrated by his 1997 essay Aggregativity: Reductive heuristics for
finding emergence. Intuitively we might think that the study of emergence should
take us directly to a case-by-case examination of those rare wholes that are obviously
greater than the sums of their parts. But Wimsatt instead turns the problem on its
headan heuristic method that we often forget to apply. And according to Wimsatts
rules, the upside-down mode is in this case more parsimonious than the intuitive one.
Instead of seeking wholes that are greater than the sum of their parts he seeks wholes
that are mere aggregates. When these are subtracted, the remainder are assumed to
have emergent properties. The properties of a mere aggregate are independent of
variations in its components, since the latter do not interact. The nature of the whole
can be discovered by testing the effects of intersubstitution or rearrangement of parts,
the effects of addition or subtraction of parts, and the effects of decomposition or reag-
gregation of parts. If none of these have any effect on the properties of the whole, it
is an aggregate. If the whole has non-linear emergent properties arising from interac-
tions between the components, some or all of the three tests will cause identifiable
change in the original system.53 (I have adjusted his categories slightly to isolate the
test conditions from the processes of interaction.) This approach demonstrates that
mere aggregates are rare, even outside biological systems. Artifacts dont count since
human emergent properties are involved in their construction. Accordingly, wholes
with emergent properties that dont meet the test for simple aggregates, must be
universal. Furthermore, Wimsatts three test categories suggest direct mental and
practical experimental approaches to emergence. Yet, he cautions, we tend to start
with simple models of complex systemsmodels according to which the parts are
more homogeneous, have simpler interactions, and in which many differentiated
parts and relations are ignored (Wimsatt, 1980)models which are more aggregative.
But then as our models grow in realism, we should both capture more properties, and
see more of them as organization dependentor emergent.54
Jeffrey Schwartz
Schwartz enters the fray with Sudden Origins: Fossils, Genes, and the Emergence of Species
(1999). It is inadequate to label him an anthropologist, since his interests in biology
and paleontology are profound. The aforementioned title is one that leaps off the
bookstore shelf at someone such as myself, though I do not ascribe to the idea that the
emergence of species is fundamentally important (q.v. chapter 11). Furthermore,
although he writes about emergences as sudden events, he uses the word emergence
casually rather than formally. Nevertheless, Schwartz recognizes that molecular
biology has provided us with the information that could rationalize saltatory
emergences, or hopeful monsters, especially the discoveries of regulatory Hox genes
that I have outlined in chapter 6. He also appreciates that regression or deletion of
gene expression has been important in the diversification of clades. I would only
complement that notion with the proposal that orthogenesis/allometry, has been
responsible for the exaggeration of what remains after deletion.
Peter Corning
Peter Corning has also addressed emergentism as a subset of a larger Synergism
Hypothesis (1998). This is a valiant attempt to encourage the expansion of interdis-
ciplinary thinking through the recognition that most of life and much of non-life is
founded upon synergistic interactions. It is interesting that a complexity theorist can
remark that in contrast with the bloodless mathematical caricatures that are blind to
the functional properties of the phenomenal world, the synergy paradigm draws our
attention to the function aspect of cooperative effects.55 Corning has also escaped the
domination of natural selection found behind the Looking Glass. He clearly states that
natural selection is the effect of emergent change:
. . . causation in evolution runs backwards from our conventional view of this in evolution,
functional effects are causes. To use Ernst Mayrs (1961) well-known distinction, it is the
proximate functional effects which result from any change in the organismal-environment
relationship that are the causes of the ultimate (transgenerational) selective changes in the
genotype, and the gene pool of a species.56
The larger category of synergism makes sense in the general context of evolution.
Although emergentism is a subset, and an important one, emergent change is followed
by a new dynamic stability. Both are synergistic, and both are part of the persistence
and progress of life. Corning is especially taken with symbioses and social interactions
that have unique properties arising from their emergence. Nonetheless, he extends
synergism to include non-living complexes as well.
When we consider pioneering thoughts about the nature of whole, we have to
remember that Aristotle observed in Metaphysics that the loss of a single part may
destroy the whole. Corning calls this the synergy minus-one methodology for
testing synergy. He notes that in many biological examples the loss of a DNA base, or
a protein amino acid, or a transfer RNA, or an endosymbiont, will bring about the
collapse of the whole. This echoes Wimsatts test for an aggregatetake away a bit and
nothing happens. So a population is an aggregate? A school of herring is behaviorally
synergistic. Nevertheless, as Corning says, if a predator eats a herring from a feed ball,
the whole is not destroyed, only diminished. But gobble a lot, and the population may
be reduced to less than an effective breeding group. And even a breeding group resists
a clear-cut distinction between aggregate and whole. It only takes two to tango,
318 Chapter 8
although two, by themselves, are deficient in biodiversity, and have a high probability
of extinction. This train of thought brings us to the perennial debate over V. C.
Wynne-Edwardss 1962 Group Selection Hypothesis. Corning proposes that the
rehabilitation of the group as a selective unit is justified on the grounds that there are
mutually beneficial synergistic interactions between members of a group that are not
close kin.57 Although I will delay dipping a toe into these muddy waters until my final
chapter, I should register my agreement, and add that Corning also suggests
comparative biological studies that would demonstrate that large groups operate more
efficiently than small groups.
Corning develops these ideas further in Natures Magic: Synergy in Evolution and the
Fate of Humankind (2003). He continues to regard emergence as an important subset of
synergism, but dislikes the term because of its plethora of synonyms. Although he
gives natural selection more prominence in evolution than I do, there is considerable
overlap in what we both find interesting in biological emergences. He emphasizes the
proposition that behavior is a primary, though proximate cause of evolution, but takes
no account of the physiological foundation of behavior.
Harold Morowitz
Just when I thought I had completed this chapter, I encountered Harold Morowitzs
The Emergence of Everything: How the World Became Complex (2002). Although he does
indeed address all of the important emergences in the broadest sense, from the Big
Bang to mind, he is not guilty of constructing a theory-of-everything-that-turns-out-
to-be-a-theory-of-nothing. Indeed, he does not construct a theory of anything; but
manages to reinforce the concept of progressive complexification of the Universe
through the emergence of the elements and their compounds, and novel chemical
properties in general; the emergence of geospheres; life; membranes; metabolism;
eukaryotic cells; multicellularity; nervous systems and intelligence. However,
Morowitz runs into the same problems as Robert Chambers, Henri Bergson, C. L.
Morgan, Samuel Alexander, and Jan Smuts. Since God is in their metaphysical
machines, He, She, or It must have been there from the start. Chambers (1844) had
God create a Babbagian computer program that produced apparent novelties that were
really part of the original divine algorithm. Bergson (1908) began with a primordial
consciousness that leapt in vital sparks to greater complexities. Alexander (1920)
made God both the creator and the fabric of the cosmos, but regarded Deity as
emergent from life. For a more comprehensive treatment of these implications, see
chapters 5 and 6 of my 1985 book Evolutionary Theory: The Unfinished Synthesis.
Morowitz, though very well qualified to elaborate mechanistically on the ascending
hierarchy of emergent levels in physics, chemistry and biology, has created the same
difficulties as the transcendentalists. As a result he is forced into a contradiction in
terms by making the Universe unfold, despite his opinion that emergences are
unpredictable events with novel properties. And eventually he retrenches into a

hylozoic/panpsychic position that mind is not, after all, a sudden emergence, but a
property of cosmic maturation. Mind emerges over a long time, not just over the last
500 million years. It is more deeply embedded in an evolving universe, and may have
prebiotic roots.58
Overview of Emergence
Types of Emergence
Developmental changes dominate the scheme of emergent evolution that Mller and
Wagner present. But before epigenetics or morphogenesis became significant, life
emerged, biochemical networks complexified, prokaryotes symbiosed, sexual repro-
duction originated, and simple multicellularity arose. Physiogenesis and the
physiological and behavioral responses of organisms that accompanied developmen-
tal evolution are insufficiently explained by epigenetics. And societal relationships are
largely independent of them. Nevertheless, Mller and Wagner provide principles that
apply beyond developmental evolution. Therefore I incorporate them into a system
based on my own interpretations of what has been suggested in the past.
Although it is not the universal cause of emergences, reproduction is what makes
them persist. Reproduction also contains processes that provide for evolvability. The
kind of molecular reproductive apparatus needed to faithfully pass on some of the sur-
vivability of the parent to the offspring has to be able to make a copy of itself. Along
with the flexibility to come apart temporarily for copying, comes the opportunity for
the production of copies that are not exactly like the original, hence differentiation.
Thus, the unavoidable consequences of reproduction are duplication and variation of
the parental units. These natural experiments are complemented by a basic emergent feature
of sexual reproductionevery generation is required to begin from scratch at the single cell
stage. This makes it possible to progressively reorganize dynamic structures during the entire
course of an organisms individual development. In contrast, if it reproduces asexually, the
existing components cannot be radically reorganized. However, adding on new
features to actively growing or established organisms is not out of the question
especially in plants. Growing roots are epigenetically altered to make nodules that
accommodate symbiotic nitrogen-fixing bacteria. Growing shoots in contact with
damp soil put out roots instead of leaves. And somatic mutation can change the
structure of new shoots and can be passed on to the next generation. Are such changes
to be characterized as continuous or discontinuous?
Saltatory Emergences
In the sense that they are discontinuous, changes within organisms are almost all
saltatory. A point mutation may produce a protein with a new function without any
320 Chapter 8
half-measures. However, I reserve the epithet for emergences that appear suddenly
from radical complexifications and re-organizations. Although the emergence of life
and mind are likely in this category, it is more tangibly exemplified by the endosym-
biotic association of prokaryotes to produce the first eukaryotes. It has all of the typical
connotations of emergence: unpredictability, greater adaptability, multifunctionality
a whole that is greater than the sum of its parts. This implies an adequate integrity at
the point of emergence, causally prior to the involvement of the syndrome of natural
selection in adjusting the self-organization and coordination of the new whole.
Contingent associations of organisms, or molecular modules that had evolved inde-
pendently, are clearly important constituents of saltatory evolution. So too are the
emergences of hopeful monsters due to epigenetic changes. Backing the success of
hopeful monsters is physiological, and hence behavioral adaptability. Environmental
factors may catalyze saltatory emergences, for example, the availability of significant
others for association, or physicochemical stimuli that may trigger chain reactions.
Saltatory emergences are the most radical evolutionary changes.
Critical-Point Emergences
These may arise from thresholds in otherwise continuous epigenetic processes. Since
critical-point emergences lend themselves to selectionistic interpretations I allow
them a longer discussion than saltatory emergences. They may involve allometric or
orthogenetic continuities of change in functional anatomy, as exemplified by the
acquisition of true winged flight. The story of wings in the higher vertebrates brings
in several interesting corollary aspects of emergent evolution. Knowing how the
primitive vertebrate forelimb began as a swimming organ, and then became a creeping
or walking organ, it is difficult to conceive of a hopeful flying monster appearing with
fully developed wings, due to an all-or-nothing epigenetic event. Nevertheless, the
flying reptile Coelurosauravus jaekeli supported its wings with rod-like bones that were
not derived from pre-existing structures like forelimbs or ribs. Instead they arose de
novo from dermal mineralizations, like battens in a sail, possibly because of physical
lines of stress along which chondroblasts migrated and differentiated.59 As was
mentioned in chapter 5, the universal pteroid bone that supports the proximal leading
edge of pterosaur wings probably arose in the same way.
The repression of Hox gene expression has been attributed to the simplification of
the proto-dinosaur forelimb that led in one direction to bird wingsand could have
been an all-or-none event.60 An allometrically growing, incipient, feathered wing
would soon have gained an intermediate plateau of adaptability. It had multifunc-
tional potential as a grasping hand, a balancing organ associated with rapid bipedal
running or arborealism, and as a net for pulling insects out of the air.61 Even when the
wing has been fully adapted for flight it can do other things. A bat can use its wing
like a catchers mitt if the insect is not immediately seized by the mouth. And what
better way to go after flying prey than to take to the air? The proto-bat could figure
that out for itself without the imaginary urging of selection pressure. Like the
pterosaurs of the Jurassic, the New Zealand short-tailed bat Mystacina tuberculata
continues to use its wings for terrestrial locomotion, having in this case gone to
ground to forage for insects in leaf litter. I once saw a crow brought down in a pond
by vengeful young ducks who had suffered the attacks of crows since fledglings. It
painfully but effectively sculled its way to shore with its wings. As Darwin observed,
the water ouzel, or dipper, can effectively fly underwater to forage. And the
penguins wing was exapted as a flipper. Oddly, some flightless birds retain vestigial
wings that have no apparent function. One might think that selection pressure would
have turned them into something useful!
Gliding and soaring could have arisen as the first critical-point emergence made
possible by continued expansion of the wing area. Once gliding became a habit, lift
would exceed the pull of gravity at the next critical point in allometric modification,
through a combination of the expansion of wing area and flappability. Beyond that
critical point true flight was an instantaneous reality. The new habit freed insects from
predators and gave easy access to tall plants and their energy-rich reproductive organs.
This aerial plankton was an extra attraction for birds and bats.
These examples show that the generative conditions for emergences are combina-
tions of epigenetic molecular changes, developmental shifts, and alterations of
habitat, physiology and behavior. As organisms evolve progressively they explore new
environments where restraints are different, behavioral choices wider, resources
greater and competition in abeyance. From the association of organisms there arise
social organizations that are greater than the sum of their individual members. Their
emergent properties feed back to affect the individuals that constituted their
generative level.
Critical-point emergences in evolving organisms were conceptualized first by C. L.
Morgan, but complexity emergentists frequently cite examples in non-living systems.
Nicolis and Prigogine (1977) found that Bnard cellscolumns of rising warm water
surrounded by sheaths of descending cold waterform at a critical temperature point
in the heating gradient. Per Baks theory of self-organized criticality arises from the
same kind of inanimate phenomena.62 But applying it to evolution in How Nature
Works (1996), he assumes that the build up of self-organization is due to the
cumulative selection of adaptations. Moreover, at the critical point the build up is dis-
integrative, and his biological examples deal with extinction rather than progressive
self-organizing evolution. He also concludes that exogenous catastrophic events like
impacting asteroids are irrelevant to major extinctionsthey would happen anyway
as the result of minor disequilibrating events when critical points had been reached as
a result of continuous selection! We think of continental drift as a gradual process on
a geological time scale. But it too was probably punctuated by critical points where
322 Chapter 8
traditional movements of animals, and the dissemination of plant spores and seeds,
stopped or began relatively suddenly. Indeed the impact of such geomorphological
effects has been held responsible for major diversifications in marine invertebrates,
birds, and mammals.63
The Causes of Emergence

The causes of emergence are the causes of evolution. My use of the term natural
experiment is intended to move the focus of attention toward the origins of
biological novelty, and away from natural selection or sorting. It embraces all the
causes of emergence as well as the origins of simple, adaptational modifications. If the
question of how emergence occurs does not immediately elicit blinding insight, it has
to be approached the hard way with analysis and categorization of evolutionary
changes. This is the epistemological route chosen by Aristotle when he constructed
the scala naturae, and developed by Francis Bacon in Novum Organum (1620) on the
grounds that tabulation organizes phenomena, and allows the detection of hidden
relationships.
The most important natural experiments can be separated into three arenas of
operation: the associative, involving intimate symbioses and social interactions, the
physiological and behavioral, and the epigenetic, or developmental, which includes
anatomy. All of these causal matrices are mutually influential. Moreover, they operate
in, and are causally connected with the environments of cells, the organisms internal
milieu, and the world at large. Environmental influence is accommodated under
extrinsic emergences.
Intrinsic and Extrinsic Emergences

Saltatory and critical-point emergences can be re-sorted according to whether they
arise autonomously within a single organism (albeit through changes in part passed
on from the previous generation), or through the interaction of the organism with
external physicochemical, organismal, or ecological systems. C. L. Morgan used
immanent and transeunt, but intrinsic/endogenous/autonomous and
extrinsic/exogenous are less portentous to contemporary ears. Saltatory emergences
come from both intrinsic and extrinsic generative conditions. Critical-point
emergences tend to arise internally but they progress in relation to behavior and the
conditions of the external environment. These two basic categories are therefore never
mutually exclusive.
Intrinsic Factors
Some mechanisms may act spontaneously within the organism to produce emergent
novelties affecting symbiosis, epigenesis and physiology. These include the following:
point mutations of structural DNA
exon shuffling and consequent alterations in primary protein structure
contingent recombination of structural genes and, consequently, protein domains
mutations of modifier or regulator genes
modifications of transcription and translation mechanisms
transpositions, and resultant alterations in gene expression
changes in methylation and histone-binding patterns,
duplications of codons, exons, genes, chromosomes, genomes
repetitive differentiation
alterations of repair mechanisms
self-amplifying holons that produce allometry/orthogenesis
structural reorganization of the cytoplasm of gametes, especially ova.
Although these are intrinsic occurrences, an extrinsic mutagen or trigger is sometimes

involved. Once they occur, they will persist if they are adequately integrated into the
organism. But even enhancement of overall adaptability may be of no particular use
during the lifetime of the novel emergent. Either way, immediate improvement in
fitness compared to the parental type is not assured; life might be precarious until the
new system has been fine-tuned, and here natural selection qua dynamic stabilization
has a role to play.
Intrinsic experiments in emergent evolution that occur without reference to any
extrinsic factors are the focus of complexity or antichaos theory. Stuart Kauffman
asserts that most organized complexity arises from tendencies for innate order to
emerge in complex interactive networks.64 Anticipated by Lamarck, Mivart, and
Bergson, this also follows logically from an understanding of the nature of the
molecular reproductive apparatus, even for biologists who are not up on history or
chaos theory. If formal laws of innate complexification were to be framed, gradual
trend to critical-point emergence would be a strong component, but some major
saltatory emergences catalyzed by contingent effects from outside the organism would
324 Chapter 8
be excluded. A prokaryote cell could not have become a eukaryote unless there were
other independently evolved, potential partners out there.
Extrinsic Factors
Environmental influences fall into two groups. The first have a broad impact, such as
physiogeneses that alter the internal milieu, or affect functional anatomy. The second
category consists of specific external environmental stimuli that trigger change in
DNA expression, which may affect epigenesis. Development and physiology can be
affected by the environment above the DNA level, and such changes might be
converted to internal adaptations under genetic control. These are not just physical
factors like light, temperature, and humidity but also more complex biological factors.
Availability of food and consequent egg size affects development. Overcrowding
makes salamanders into monstrous cannibals, and causes locusts to change color,
enlarge their wings, and take to flying in swarms.64 Interspecific factors include free-
living bacteria that affect thallus form in seaweeds, nodule formation in legume roots,
and gut development in mammals. Genetic assimilation can fix environmentally
imposed change, in both developing and mature organisms. As Schmalhausen and
Waddington realized, this leads to internalization of environmental stimuli of
development, and ultimately tighter canalization. It presupposes an alchemical
cauldron in the basement, seething with molecular experiments. Its products might be
shelved, or recycled, or might just be immediately usable as a generative condition for
a higher level in the organismal and environmental hierarchy. One consequence of
the interaction of intrinsic and extrinsic mechanisms is increased adaptability and
hence greater organismic integrity, but fixed adaptations or specializations can also be
produced.
In animals, the freedom conferred by adaptability permits behavioral experiments,
and wider explorations of more extreme environments. Thus, there is a strong positive
feedback loop with the environment that may bring about even more internal change.
Adaptability in plants is partly physiological, but their strongest feature is ontogenic
plasticity. A terrestrialized reproduction is important, and is linked with the
exploratory behavior of pollinating animals. Prokaryotes have the adaptability to
acquire additional genes by various routes, but endosymbiotic gene acquisition by
eukaryotes was one of the most important evolutionary improvements in the adapt-
ability of individual organisms. In symbioses the qualities of the participating partners
complement each other, and in social interactions within groups of higher animals
there is a parallel complementarity of both genetically and traditionally inherited
talents.
In the face of environmental changes the syndrome of natural selection may
tolerate adaptable generalists over many generations. David Rollo suggests that
strategies that ensure being approximately right most of the time are favored over
those that may be locally superior, but that also run the risk of being precisely
wrong.65 Nevertheless, under stable conditions, specialists may continue to be
precisely right for very long periods. Adaptable organisms must then hang on at envi-
ronmental fringes and interfaces that fluctuate both rhythmically and irregularly, and
where there is little competition. But to thrive they must have an emergent quality of
unusual utility, or risk new environments, or find old environments that have been
cleared of competition. Thus, the sense of physical movement from one environment
to another is central to the concept of emergence.
The separation of emergent phenomena into the intrinsic and the extrinsic is a
simplifying exercise, but forgetting to reunite them in the final analysis is counterpro-
ductive to the quest. How well have complexity theorists succeeded in integrating
intrinsic and extrinsic events that effect emergences? Kauffmans generalization about
evolution through cell differentiation is succinct but exclusive of environmental causes:
. . . the existence of distinct cell types, the homeostatic stability of cell types, the number of cell types
in an organism, the similarity in gene expression patterns in different cell types, the fact that
development from the fertilized egg is organized around branching pathways of cell differentiation,
and many other aspects of differentiation are all consequences of properties of self-organization
so profoundly immanent in complex regulatory networks that selection cannot avoid that order. All
aspects of differentiation appear to be properties of complex parallel-processing systems lying in
the ordered regime. These properties may therefore reflect quasi-universal features of organisms
due not to selection alone, but also to the spontaneous order of the systems on which selection
has been privileged to act.66
This is an illustration of how constant genuflection to natural selection, even if

ritualized to a momentary dip, gets in the way of a good ground-breaking stride.
Holland also largely omits extrinsic factors. Yet, autonomous (intrinsic) self-ordering
is a multiplex process that is difficult to isolate from the whole causal matrix.
Matsudas work, and more recent books by Rollo, Jablonka and Lamb, Hall, Pearson,
and Mller, and West-Eberhard, amply illustrate how the emergence of new orderings
in the epigenetic arena are so often dependent upon external events. The simple avail-
ability of food, which might provide for larger eggs, is enough to trigger epigenetic
novelties. The lack of an element in the food, for example iodine needed for the
synthesis of thyroxine, may be enough to induce neoteny in an amphibian. The
presence of a hormone in a juvenile termites food at a particular time of development
determines its caste. In some cases environmental effects impose epigenetic
regressions that are then followed by natural experiments with novel autonomous
products.
In the present book, I have gone beyond Schmalhausen and Waddington to show
that the evolutionary path of animal homeostasis at the organism levela paradig-
matic self-organized complexityhas been dictated in part by physiogenic changes
induced by the environment. Some emergences are contingent upon the co-existence
326 Chapter 8
of other independently evolved systemsproto-mitochondria and proto-chloroplasts

had to evolve independently and then come together in the same place and at the
same time to give rise to endosymbiotic eukaryotes. Some are profoundly influenced
by catastrophic events. Natural selection is not involved in any of these except as a
post hoc stabilizing influence.
Some physical emergences into different environments, as well as evolutionary
emergences, may be simply intolerable to the continued integrity of the emergent.
They may also be rebuffed by the agents of natural selection, so that if the novel
organisms are not strongly benefited by an immediately beneficial feature of the
emergence, they will be unsuccessful in the face of competition. On the other hand,
their progressive adaptability can operate in fluctuating environments, or in new envi-
ronments where the established order of competition and predation do not exist, or
where there has been a catastrophic environmental change that leaves the field open
for new players. Catastrophe and emergence go hand in hand, and David Raup has
gone so far as to suggest that progressive evolution would have been impossible on a
planet that had not been subjected to major bolide impacts, however devastating they
were in the short term.67
Emergences in Relation to Progressive and Adaptational Evolution

In categorizing emergent evolution into saltatory and critical-point, and
intrinsic/extrinsic events, it must not be forgotten that evolution is both progressive
and adaptational. Progressive evolution involves the emergence of new levels of
complexity/self-organization/adaptability. It is followed by a phase of diversification,
involving orthogenesis/allometry, and specialization of habit in relation to habitat. I
only need to confirm that all categories of emergence are involved in progressive and
adaptational evolution, with a larger component of intrinsic/saltatory emergence in
progress, and a larger component of extrinsic/critical-point emergence in adaptation.
Stases
As I use it here, the word stasis does not mean inertia, low entropy, or the arrest of
time. In each causal arena where emergences persist, new dynamic equilibria develop
around them. If variant properties that are adaptational to the newly emergent
condition are selected, it is on the basis of integrative harmony and energetic
efficiencywhat Brian Goodwin simply calls quality. Natural selection, along with
its agents, is the hypostasis of a stronger dynamic stability. By analogy, consider
Genghis Khans conquest of China. The existing bureaucracy quickly re-arranged itself
out of disarray to support the new dynasty, and thereby helped to ensure its sway for
several centuries. Formerly resistant to change, the mandarins served to consolidate
the revolution and to protect the new order from further encroachment. As time
passes, stases become stronger and more resistant to the further modification. The
most familiar are homeorhesis in the epigenetic arena, homeostasis in the physiolog-
ical arena, and ecostasis in the environment at large. Symbiostasis is the parallel
stabilization of associative relationships and it demonstrates that evolution can
progress despite stasis. Stasis is actually in a constant state of fluxthe Red Queen is
always running, and minor natural experiments lead to minor adaptations, without
achieving any progress, although the Ultras call it evolution. The worldviews of uni-
formitarianism and gradualism were persuasive because stasis is the prevailing
condition of life. Subjectively, as an organism, I would prefer to continue in stasis,
rather than to live in interesting timesas the Chinese curse has itwhen I might
not survive long enough to enjoy the stay.
For traditional evolutionists, what happens now is the model for evolution as a
whole, and since stasis is the prevailing condition they must somehow explain it as
evolutionary. Anything tainted with sudden change, catastrophe or saltation, is
anathema. Those who have canonized natural selection might see its re-invention as
hypostasis to be an act of destruction. However, they should be grateful to the
originators of punctuated equilibrium for tacitly ceding to natural selection a
significant role in punctuation as well as the major role in equilibrium phases.
Moreover, there is a significant role for its hypostasisgenerative entrenchment of
dynamic structure provides a platform that can be built upon, although its destabiliza-
tion has often been part of progressive emergence.
Evolution would never have occurred if the motor of adaptation were the driving
force, for its square wheels stop it as soon as it turns over. But the investigation of stasis
is not superfluous to evolutionism. Knowing what blocks evolution helps us to
understand what causes it, and it is useful to know that a period of relative stasis gives
a better guarantee that new emergents will be internally well adjusted. Here are the
tableaux vivants of stasis found in the rings of the evolutionary circus:
1. Symbiostasis. It may be extremely robust, or very vulnerable to change. Once

entrenched, eukaryotic symbioses were never abandoned, remaining intact in the evo-
lutionary lineages that possessed them and built upon them. Looser associations are
more fragile, and may easily be destroyed, because harm to one is harm to both. Social
emergences with innate behavior patterns tend to be inflexible but their members can
be sacrificed without serious detriment to the whole society. At the human level a
reservoir of adaptability resides in an array of independent individuals, which offsets
the inflexibility of traditional behavior patterns.
2. Homeorhesis. The build up of developmental stasis results in tight canalization, with

epigenetic locks that prevent disequilibration and keep the organism true to type. The
archetypes of animal and plant morphologies may all have arisen at a time in
biological history when canalization was loose, and natural selection in abeyance.
328 Chapter 8
Once established, homeorhesis could not easily be overridden. There remained

potential mechanisms of epigenetic evolution, such as paedomorphic regrouping,
hypermorphic additions, heterochronic alterations and radical deviations. Gene drive
could overcome homeorhesis sufficiently to cause allometric shifts.
3. Homeostasis. Disequilibration of the internal milieu by physiogenesis overcame the

weak resistance of homeostasis in early aquatic animals. Changes of this kind, though
random, demonstrate the positive feedback loop between physiological adaptability
and behavioral versatility. Commitment to terrestrial living locked in the chemical
composition of the internal milieu as it was when the primitive tetrapods emerged
onto land. It also potentiated more sophisticated self-organization, because the greater
availability of oxygen levels could sustain the high metabolic rate ultimately provided
for by homeothermy. Progressive improvement of homeostatic organization helped
emergent organisms to diversify through a wider environmental range, since they had
become more and more independent of the external milieu. Natural experimentation
with behavior has been subject to stasis, through genetic fixing of patterns and loss of
flexibility. In mammalian lineages freedom of choice has expanded, although traditive
behavioral patterns in humans can be as rigid as genetic fixation.
4. Ecostasis. In the world at large, the resistance of natural selection to change was
often overcome by ecological destabilization, which removed competitors and
predators of emerging evolutionary novelties. Some hopeful monsters that emerged
from natural experiments were only able to diversify after catastrophic, mass
extinctions. Which of those succeeded might have been simply a matter of luck, of
emerging in the right place at the right time. But the more adaptable the organism is,
the more likely it is to arise like a phoenix from the ashes.
Although this chapter illustrates how emergent phenomena have been given serious
consideration by materialistic biologists, it also illustrates how adherence to selection-
ism limits emergentisms analytical and creative scope. Most progress has been made
by those who merely pay lip service to the role of natural selection, who ignore it
entirely, or identify themselves as Contras. In the following chapter I will round up
the causal particulars of emergence to establish additional generalities, and discover
how feasible an emergence synthesis might be.
9
From the Particular to the General
We can only augur well for the sciences, when the ascent shall proceed by successive steps,
without interruption or breach, from particulars to the lesser axioms, thence to the intermediate,
and lastly, to the most general.
Francis Bacon, 16201
Francis Bacon was more a gradualist than an emergentistno revolutionary interrup-

tions or breaches for that staunch supporter of a stable monarchy. Yet the many
relevant evolutionary particulars that have accumulated over the last century need
some kind of ordering. And, as Arthur Lovejoy demonstrated, a Baconian epistemol-
ogy can be just as easily applied to discontinuous evolutionary emergences as to
continuous adaptational variation. Lesser axioms pertaining to the various
common and exceptional causes, found in the causal rings of the emergence circus,
have already been sorted out. Now we can move on to intermediate inductions.
Identifying the necessary and sufficient generative conditions leads to the final goal
the most general inferences that apply to everything that is going on in the biosphere.
The Symbiosis/Association Arena
Associative emergences were the first as well as the latest stages of evolution
chemical associations gave rise to primitive cells, and humans associate in families and
societies and global networks. They can be divided into four major subsets: intraorgan-
ismal (some intracellular) mutualistic symbioses, sexual associations, differentiated
multicellularities, families/societies. There are also many loose commensal and
cleansing relationships, and a variety of co-evolutionary interactions. Endosymbioses
present us with the clearest illustration of saltatory emergence. Although the hosts and
pro-symbionts might have been in each others physical presence for a long time, they
came into a state of symbiosis suddenly, furnishing mutually beneficial qualities that
the formerly independent organisms lacked. An important emergent feature of foun-
dational symbioses is the acquisition of heritable characteristics. These make the new
330 Chapter 9
whole greater than the sum of the parts, and provide for transmission of that
wholeness directly to the next generation. When the first eukaryotic cellular
communes came into being, some features that were negative in the earlier state of
independence became positive in the context of the new whole. This emergent
property made up for the loss of independence, although, now, if something
detrimental happened to one of the partners, the other would suffer as well, a
condition that the multicellular condition was eventually to mitigate.
Eukaryotes also lost the genetic flexibility that the constituent prokaryotes had, and
still retain, in the form of transformation and conjugation. However, at the new level,
transposon flexibility still persisted, as did viral and bacterial transduction. The latter
provides a natural parallel for the genetic engineering process of transgenesis although
the magnitude of its contribution of foreign genes is not well known. Genetic
flexibility was restored in part by the emergent properties of sexual association. The
natural experiment of meiosis not only provided for increased shuffling of the genetic
deck, it also allowed the organism to identify and repair point mutations more
thoroughly.
Emergences involving multicellular associations, and their differentiation, complex-
ification and organization, belong as much to the developmental and physiological
arenas. That leaves the emergence and evolution of societies as the final performances
in the association arena. These have had a particularly strong feedback effect on the
evolution of the endocrine and nervous systems and on behavior.
Here are the aphorisms of association that will contribute to a theory of association,
and complement the developmental and physiological principles:
1. Associative emergences constitute saltations whose whole is greater than the sum of
the parts.
2. They are physiologically more adaptable than their independent antecedents since
they allow greater differentiation and coordination of functions. (Holland has cited
symbioses as unpredictable generators of enhanced persistence.)
3. Photosynthesis of prokaryotes, enhanced by endosymbioses, effected a major geo-

physiological change: oxygenation of the biosphere.
4. Sexual associations provide for more genetic mixing and matching, and hence more
evolvability, without totally sacrificing the unique qualities of the parents.
5. Sexual reproduction (as opposed to vegetative reproduction) guarantees that the

entire developmental process from single cell to mature multicell is repeated in every
individual, exposing every stage to epigenetic change and subsequent evolution.
From the Particular to the General 331
6. Although there are disadvantages that increase the vulnerability of partnerships,

some associations like eukaryotic endosymbioses have been so vital, and ultimately so
supportive of organismic integrity, that they have remained the foundation of most
living organisms and ecosystems.
7. Symbioses sometimes have mutualistic, interspecific epigenetic effects between

symbiont and host.
8. The emergence of societies whether by insects or vertebrates has tended at first to

fall into genetically assimilated, instinctive dynamic stabilities. But such fixed
action responses can be modulated and escaped. Nevertheless, the most flexible kinds
of societies are those that have arisen in placental mammals that developed sophisti-
cated nervous systems before they developed social behaviors. Thus, organisms that
have brains and plastic behavior are always adaptable, although they sometimes run
the risk of becoming creatures of habit.
9. The adaptability of human social associations generates an emergent non-genetic

freedom of choice and intelligence that cannot be fixed by natural selection, although
human societies often replace it with other rules and regulations.
10. Symbioses have founded and nurtured major aquatic and terrestrial ecosystems.
Major emergences in themselves, they brought into being the entangled bank[s], the
Darwinian symbols of evolutionary and ecosystemic complexity.2
Evolution by association evokes pithy principles: mix and match, the whole is
greater than the sum of its parts, the acquisition of heritable characteristics. And,
regarding generative conditions, being in the same place at the same time. Some of
these also apply to some of the processes of physiological, behavioral, and develop-
mental evolution. Being in the right place at the right time may be a matter of luck,
but in the course of evolution it has often been essential.
You may observe that the following arenas get lengthier treatment. This is not a
measure of their relative evolutionary importance. In a general sense, the
symbiosis/association arena might include multicellularity, but its differentiations and
their functions have been abstracted into the physiological and developmental arenas.
The Physiological Arena
First, what happened in this most ignored ring of the evolutionary circus? Some
general principles will emerge from a recapitulation of the main events. How did they
happen? What were the generative conditions and mechanisms of physiological
evolution?
332 Chapter 9
The Main Events

The coordinated properties of reproduction and homeostasis are inherent in the
emergence of life. The first cells needed enough physiological adaptability to preserve
their integrity until they reproduced, and reproducibility had to be faithful enough to
pass a genetic base of adaptability on to subsequent generations. While persistence of
an organism and its lineage can be summed up by the words survival and repro-
duction, these are emergent properties of the first living cellnot the product of
natural selection; quite the reverse.
The most primitive cells could both persist in a stable environment and respond to
changing conditions. In prokaryotes, this adaptability combined cellular homeostasis
and the genetic ability to pass on adaptational improvements located in plasmids,
through conjugation. When multicellularity emerged, the homeostatic power of
regeneration was enhanced. The wholeness of the organism could be maintained by
cell and tissue replacement. Then multicellularity took a three-dimensional form, with
an internal milieu that reduced stress on the interior cells. But the next stage of phys-
iological evolution had to accommodate to environmental change through
conformity.
Initially the physicochemical nature of the internal milieu was imposed by the
environment. Primitive vertebrates were vulnerable to osmotic physiogenesis during
their early aquatic phase. When they became terrestrial, some physical and chemical
features were locked in, but further physical changes did occur, such as an increase in
oxygen capacity, cheaper access to oxygen, and the addition of thermogenesis and
homeothermy. During all these phases, existing coordinative conditions were refined,
and innovative progressive improvements to the endocrine and nervous systems were
major emergences. The culmination of homeostatic evolution in birds and mammals
prepared them to survive major catastrophes, as well as to venture into zones that
would have been deadly for their forebears.
Independence from the environment allowed the higher vertebrates to experiment
with new habits and habitats. Novel behaviors were correlated with progressive
experiments in morphogenesis. Semi-independent features could be altered, such as
the use of the limbs for flying, burrowing, swimming,, and running. Internal organ
systems were adjusted, and the brain hypermorphosed. The quintessential feature of
progressive physiological evolution is the adaptability to keep on doing the same
things when external conditions change, and to do different things when external
conditions stay the sameand anything in between. This underpins anatomical and
behavioral specialization for specific habits and habitats. Thus, placental mammals
can get themselves into strange situations, and persist until emergent morphological
features and new behaviors are integrated. The stability of their internal milieu, in
particular the constancy of body temperature, is especially significant for the
developing embryo. The placenta allows maternal homeostasis to be shared intimately
with the developing fetus until birth at a mature stage. This new level of homeostasis
was also the foundation for the emergence of cerebral complexity and intelligence.
Generative Conditions and Mechanisms of Physiological Evolution

Biochemical novelties can emerge at any level of organization. One mechanism is the
construction of novel proteins through shuffling or differential expression of exons.
Gene sharing (i.e., combining all or bits of different genes to generate novel proteins)
is another. These rearrangements of DNA sequences could hypothetically account for
a great deal of novelty, but new proteins are relatively rare. More universally,
repetitive differentiation of genes allow the extension and branching of biochemical
pathways. These branchings parallel epigenetic bifurcations and variability. These
metabolic amplifications contributed to the homeostasis of primitive cells and of mul-
ticellular organisms operating in fluctuating environments.
When they first emerged, membrane proteins or proto-integrins of prokaryotes may
have had multiple skeletal, catalytic, and absorptive functions. Their repetitive differ-
entiations established physical adhesion among cells and between cells and
environmental surfaces. This, in coordination with contractile microfilaments,
allowed for a degree of cellular motility in multicellular organisms. Membrane
proteins also gave rise to several membrane transport mechanisms, thus setting up the
generative conditions for the evolutionary emergence of nerve cells. The (possibly
orthogenetic) accumulation of ion channels in cell membranes finally reached the
critical point where an adequate electropotential for the effective transmission of an
impulse could cause the emergence of intercellular communication. Organization of
the nervous system was made more complex by the repetitive differentiation of neu-
ropeptides and their receptor molecules. Differentiation of sensory organs and their
receptor molecules let animals find their place in nature and act appropriately.
Regression of key enzymes in the metabolic maze, whether through repression or
the lability of the responsible genes, has sometimes reinforced commitment to
particular physiological modes, such as uric acid or urea excretion. Regression of
hormones affects the options available to organisms inhabiting stable and long-
established environments. As a result of the use it or lose it effect, most fish have
regressed to the point of being unable to travel back and forth between the sea and
fresh water to visit their distant relatives. Nor is the sophisticated homeostasis of birds
and mammals immune to regressive specialization. Some or all of the time, humming-
birds, camels, bats, hibernators, and mole rats abandon homeothermy, thereby saving
water and metabolic energy.
Some inflexible biochemical novelties that are immediately useful, and normally
classed as adaptations, may also strongly enhance general adaptability. For example,
the waxy waterproofing layer of the insect integument, an adaptation to a dry
environment, improves the containment of body water. It is not physiologically
334 Chapter 9
adjustable, but it enhances the adaptability of the respiratory system, and supports
flight, which would be worthless if the insect were to dehydrate in mid-air. Water con-
servation by the mammalian keratinous skin has similar roles. But water balance in
insects requires the additional backing of physiologically adaptable Malpighian
tubules, and mammals need adjustable kidneys.
Multifunctional organs may become specialized for particular functions, or they
might go through a series of exaptations in which only one function is to the fore.
Proto-chordate feeding organs doubled as gills. From them, specialized gills and
endocrine glands emerged. Then lungs evolved from gill pouches, and diversified into
swim bladders and amphibian, reptilian, bird, and mammalian respiratory systems.
And their bony anatomy became jaws and ear bones. Organ repetition and differenti-
ation have provided evolvability and functional diversity.
Physiogenic change imposed by the environment on the whole organism has been
particularly important in some lineages. The salinity and oxygen content of the
internal milieu have been so altered, and, with the shift from water to land, gravity
affected functional anatomy. Catastrophic environmental change may be directly
mutagenic, or contingently affective. The evolution of birds and mammals was thus
influenced by the K-T and Eocene catastrophes, and the isolation of the continents in
the later phases of continental drift also must be taken into account for both diversi-
fication and protection from competition.
Behavioral evolution is demonstrably correlated with every aspect of physiological
evolution. For much of the course of progressive change in animals, behavior may
have begun as individual, phenotypic, and therefore variable responses to environ-
mental conditions. It was then largely genetically accommodated as stereotyped
patterns. For behavior to become more adaptable, genetically fixed actions, or
engrained habits, have to have some plasticity. Disequilibration of the external
environment comes into this too, by altering threshold conditions for behavioral
changes. Finally, freedom of choice depends on the complexification of the nervous
system, in the context of a dependable internal milieu. Since progressive physiologi-
cal evolution permits more flexible behavior and consequent feedback to the
organismal condition, the action of the organism guides the genetic assimilation of
appropriate qualities of its DNA. Yet this is a principle that affects development as well.
Summary of the Principles of Physiological Evolution
Generalities with a Zoological Emphasis

1. There are two kinds of physiological evolution, the progressive advance of adapt-
ability, which can be seen in toto as increasing homeostasis, and the accumulation of
genetically fixed changes that are adaptational to particular conditions of the external
and internal environments.
2. Internal adaptations consolidate advances in adaptability. But adaptational changes

will not usually create adaptability, since they substitute one condition for another,
and are static rather than flexible. Evolution goes backwards when adaptations make
an adaptable system regress to an inflexible specialized system.
3. Physiogenic changes in the internal milieu that became genetically fixed were
involved in the evolution of adaptability. Nevertheless, the physicochemical changes
that resulted do not constitute exclusive or necessary generative conditions for the
emergence of higher levels of self-organization. Octopuses progressed quite nicely,
while keeping their original internal milieux.
4. Adaptability that makes the organism independent of change in the environment

is strongly associated with the greatest potential for behavioral and functional mor-
phological diversification. Physiological emergences have been multifunctional.
5. As adaptability has evolved, the internal milieu has become more and more stable
and resistant to further physicochemical change, without, however, resisting
functional morphological progress.
6. With the independence from environmental fluctuation granted by homeostasis,

freedom of behavioral choice has led to further progressive improvement in animals,
enabling entry into novel environments, and experimentation with habits that
involved them in subsequent functional morphological evolution and ongoing
challenges to their adaptability.
7. In turn, behavioral experiments determine what is physiologically advantageous.

The organism sets those rules. As Holland says, The context in which a persistent
emergent pattern is embedded determines its function. (See previous chapter.)
Rules for plant physiological evolution are quite different, largely because of the
essential nature of the photosynthesizing chloroplast. The very small number of
animals that have acquired chloroplasts as symbiotic organelles illustrate the
limitations placed on photosynthesis by the need for freedom of motility.
8. Above the cellular level the homeostatic mechanisms of plants are limited, and they
tolerate a wide range of internal changes. Waterproofing and transpirational adaptabil-
ity minimize desiccation. To acquire water and mineral nutrients plants must root
where they germinate, and conform to the conditions of the environment.
9. A unique ontogenetic plasticity has emergedgrowth responses to the environment

persist for the life of the plant. The system is sufficiently flexible that one plant,
336 Chapter 9
having branches in different micro-environments, may have different functional mor-

phologies appropriate to their locales. (Lamarck used this to support his contention
that the organism responded to a need imposed by the environment.)
10. Part of the ontogenic plasticity of plants is the ability to reconstruct established
cellulose walls in response to light and gravity, through the mediation of hormones.
How a wall of cellulose emerged in the ancient marine unicells that gave rise to the
plants is unknown. However, it involved an increase in the duration of expression of
the gene for the cell surface synthetase, and was correlated with photosynthesis. The
cellulose wall is multifunctional, resisting ingestion and digestion, and physically
resisting osmotic lysisespecially on entry into fresh waterwhile admitting enough
light, water and mineral nutrients. Partially desiccation-proof itself, it was the
foundation for a translucent waterproofing layer over the epidermis, and had the
potential to combine in a variety of structures. Some of these were to be upright stems,
later reinforced as woody skeletons. These materials were unavailable to animals that
could not digest them nor utilize them fully until appropriate cellulolytic symbioses
emerged.
11. The functional morphology of vascular plants had the adaptability to support the
tree form. This created forest ecosystems that would not only accommodate much of
the diversity of other terrestrial plants and animals, but also had a climatic, geophys-
iological influence.
12. In one physiological feature, plants have progressed further than animals. Above
the level of the ferns, fully terrestrial sexual reproductive mechanisms have emerged,
with desiccation-resistant male gametes in pollen grains, and ova and accessory cells
that develop into desiccation-resistant, dispersible, food-storing seeds. In contrast,
terrestrial animals employ archaic fluid fertilization mechanisms that necessitate
intimate sexual conjugation.
13. Because animals are mobile, some able to fly, they can make close contact with
other organisms in awkward places, whether for sex or food. This facilitated the repro-
duction of flowering plants. Although pollen, fruits and seeds, and color and odor
attractants for pollinators were emergent novelties, their subsequent improvements
were subject to the preferences of insects.
It follows from the above principles of plant physiological evolution that plasticity
of growth, innovations in pollinator attraction and in spore, pollen, and seed
dispersal, and consequent adventures in novel environments provided the varied
contexts that determined their functions.
The very failure of animals to emulate the dry, terrestrialized reproduction of plants
necessitated the retention of a primitive animal intimacy for the intromission of
swimming sperm. This sexual togetherness then contributed to the evolution of
higher social symbioses.
Behavior
Since theories of behavior are beyond my personal mandate, the only constructive
action I can take is to integrate those aspects of behavior that I have touched upon in
relation to physiology, association, and epigenetics. Nevertheless, I have no hesitation
to jump into the thick of the fray when simplistic Darwinism is applied in evolution-
ary psychology and its anthropological equivalent. That conflict comes from the
perennial nature versus nurture debate about human biology, which places gene-
determined behaviors at one end of the spectrum, and intelligent actions at the other.
Much behavior is emergent at the phenotypic level. I have touched upon behavioral
changes that occur in relation to population density in ants. Schooling fish and
flocking birds show emergent behavior not found when the individuals are isolated.
The changes are generated from a critical number in the flock or school, combined
with the avoidance of bumping into each other. Emergent behavior can sponta-
neously occur in humans in much the same way, as in crowded sports stadiums. The
most important human example is in behavior that results from intelligent problem
solving and planning. These behaviors are non-linear and have no innate
programming.
Even if some behaviors are innate, or heritable, we have to accept that innateness
and heritability do not reside entirely in the genes. There are no genes for behavior;
genes are for proteins, and for regulating other genes. And to carry out those
functions they need to be prodded and helped by the rest of the organism. It is slightly
closer to the truth to say that there are proteins for behavior, since behaviors are
clearly catalyzed or colored by proteins such as hormones and neurotransmitters. Yet,
again, although proteins are for a wide variety of functions they are not for
behavior. They too need to be stimulated by the rest of the organism and its responses
to environmental influences. Their amino acid sequences do not contain the structure
of behavior, only functions that contribute to it.
The challenge is to link information about the functions of proteins, and the actions
of the organism in its environment, through the intermediate neuronal and hormonal
sensitivities and flexibilities. Unquestionably there are organisms that exhibit little
more than innate, automatic activities. And in simple organisms the links between
stimulus and response have been worked out in terms of receptors, neuroanatomy,
chemical messengers, and locomotory coordination. In some more complex
organisms too; insects and birds, for example; there are inflexible instinctive behaviors
338 Chapter 9
that serve them well under the normal conditions of their life. Despite the advantages
of flight, it limits body size and the ability of the ganglionic centers to expand to the
point where greater freedom of thought and actions are possible. Instinct is an
efficient way of packaging fast behavioral responses into small nervous systems, so
long as the conditions of life remain the same. Since they do change, it is not
surprising that birds and even insects are not complete automata, but have a measure
of behavioral adaptability. Flexible exploratory actions are essential for finding food,
shelter and mates, regardless of phylogenetic affinities.
Complex innate behavior patterns provoke the question of how they came to be
that way. Ethologists, whether genocentric ultra-Darwinists or not, would hardly
accept that a complex gene-determined behavior pattern could appear as a saltatory
macromutation or random combination of genes for behavior. By the Darwinist thesis,
the buildup has to be gradual: one gene influences a little bit of behavior which is
selected, another gets added on, and so a complex behavior pattern is constructed. The
other alternative, one proposed by many ethologists, is that the behavior is initially
very plastic and exploratory. The individual organism experiments by trial and error,
and repeats those behaviors that bring food, shelter, or mates. Then genetic assimila-
tion occurs through to genetic, epigenetic, and physiological experiments. This is the
kind of process Jean Piaget outlined in Behavior and Evolution (1979). (Piaget would be
historically classified as a structuralist, which is almost an emergentist.3) He also
inferred that the greatest variety of experimental behavioral initiatives would occur on
entry into new environments where the agents of natural selection were weak.4
From the adaptationists point of view, the success of particular behaviors that had
become genetically fixed would be complemented by the kind of eusociality found in
insects. Not only would every member of the society have the advantageous behavior;
there would also be the potential for repetitive differentiation into castesseparation
of offices and concurrences of efforts. We should however, keep in mind that those
castes are determined by ontogenic hormonal manipulation. Moreover, the birds do
very well without being eusocial. The birds and insects, despite some flight-associated
convergences are also distinctively different physiologically.
Some ethologists, including Gilbert Gottlieb (1976, 1992) and Simona Frankov
(1987), have seen parallels between behavioral and epigenetic evolution in terms of
constraints, plasticity and canalization. And the argument of Stuart Newman and
Gerd Mller (2000) that in epigenetic evolution the genomic role is to finally
consolidate the processes that began as individual organismal experiments echoes
Piagets view of behavioral evolution. So the process has parallels with evolutionary
changes in epigenesis. Another common feature is the possibility for behavioral, and
physiological changes at developmental thresholds which Eugene Balon has
emphasized in his ichthyological discourses. No matter how genetically fixed the
behavior of our fishy ancestors was, they had to have kept their options sufficiently
open to invade the freshwater environment and to allow for their descendants
becoming terrestrial.
Now, how evolvable is behavior that has become entrenched, or instinctive?
Presumably our ancestors among the mammals, reptiles and amphibians had more
stereotypical behavior patterns than we. And perhaps, up to a point, we retain more
of that kind of behavior than we would care to concede to the evolutionary psychol-
ogists. In physiology, fixation of homeostatic functions began early, though the
physicochemical milieu was subjected to a series of physiogenic alterations resulting
from behavioral and consequent environmental changes. Behavior changed the
internal milieu and its physiological capacities. But the final entrenchment of
emergent placental homeostasis was what gave the placental mammals their major
boost in epigenetic, anatomical, and behavioral diversification and freedommore of
a slingshot than a bootstrap.
While there are innate, though variable, factors of neuroendocrinology in the
evolution of human familial associations, individuality and freedom of behavior has
been retained. The playfulness of the young has been extended into adulthood. These
freedoms have allowed us to enter into broader social relationships that are both
flexible and fragile.
The Developmental Arena
Although the separation of the physiological arena of evolutionary causality from

developmental physiology and morphogenesis is somewhat arbitrary, there is one
striking distinction. Homeostasis in the mature organism is a relatively steady state of
physicochemical and biotic conditions in the internal milieu. It is the foundation of
diversifying evolution and potentiates further progressive evolution as well.
Homeorhesis governs a chronological sequence of changes in gene expression, and in
cellular differentiation, as well as in the internal milieu, resulting in a mature
organism that is larger and more complex than the egg from which it came, while
keeping it true to type. The tighter that control, the more difficult it is for epigenetic
evolution to occur. Entrenchment of generative interactions, and strict canalization
dominate epigenesis, though they can be supervened by novel additions or regressions
in the late stages of development. However, innovative morphogeneses deep within
development are known to produce cenogenic novelties of larval form and behavior.
And some radical deviations that affect the whole life history can be detected. Also,
many experiments involving the addition or removal of non-genetic materials and
stimuli demonstrate that interference with morphogenesis sometimes changes the
final product, without detriment to the organism. Natural evasive tactics such as pae-
domorphosis permit escape from generative entrenchment and tight canalization,
allowing freedom to experiment with diversification.
340 Chapter 9
From a host of enlightening books and articles on epigenetics I will single out only
one here, since it was the inspiration for the organization of this chapter. The novelties
defined and detailed in Gerd Mllers essay Developmental mechanisms of the origin
of morphological novelty: a side-effect hypothesis (1990) are essentially epigenetic
emergences. Mllers aphorisms blaze a trail toward an evolutionary theory of
development:
1. Novelties are defined as qualitative morphological changes with a discontinuous

deviation from the ancestral state.
2. The majority of novelties arise as secondary by-products of epigenesis that appear

when quantitative modifications of developmental processes reach a threshold of the
affected system.
3. The causality for the origin of novel structures lies not within the genome but in
epigenesis.
4. The specificity of morphological innovations depends on the reaction norms of

developmental systems at their limits.
5. Intermediate structures and sequential switching of mechanisms provide opportu-

nities for novelties to arise.
6. The plasticity prevailing at all levels of developmental systems facilitates the

epigenetic integration of novelties.
7. The mechanisms named share a potential for rapid morphological transformation

which may underlie several discontinuous phenomena of the evolutionary record.5
Mller is dealing specifically with morphogenesis, so a few additions are needed. At

this stage in his quest, the role of natural selection in consolidating homeorhesis, or
tightening canalizationhence reducing evolvabilityis ignored, and environmental
influences are not elaborated. The nature of epigenetic plasticity cited in aphorism 6
needs explanation, and specific molecular mechanismsin contrast to morphological
mechanisms of developmental evolutionare missing. Heterochrony, though implicit
in item 7, could also be more explicit. However, he makes up for this in a subsequent
essay co-authored with Gnther Wagner in 1991. Cases that they cite include changes
in the timing of cell lineage segregation in blastomeres of direct developing embryos,
which lead to novel forms in nonfeeding larvae. Some primitive larval features are
eliminated, and others appear earlier than usual.6 Also, skeletal evolution in vertebrate
limbs has involved heterochronic simplification as well as innovative repatterning

through dissociation and recombination events.7
According to aphorism 2, the majority of epigenetic novelties arise from a previous
continuity of change, and so they fit the category of critical-point emergence.
Discontinuous phenomena, or rapid morphological transformations, appear in
aphorism 7. Paedomorphosis alone is a saltatory change, a regression, but without the
loss of redundant DNA and associated molecular mechanisms. Those can be retooled
for new functions. Other saltatory changes are progressive, such as topographic
relocation of primordial cell lineages with epigenetic effects. These changes seem to be
buffered by developmental plasticity, which Bateson called the accommodatory
mechanism . . . not generally recognized as existing, though when stated it seems
obvious.8
Associated with this is William Wimsatts generative entrenchment, which refers
to a dynamic stability that results in canalization and resists evolutionary change. The
degree of entrenchment relates to the scope and structure of dependency relations
among the parts of a system and the environment9:
The very existence and structure of dependencies in developmental programs is the metacondition
that makes contingencies (and history) important in evolutionthese contingencies, or those of
other interacting lineages. Features (whether contingent or not) that accumulate many downstream
dependencies become deep necessities, increasingly and ultimately irreplaceably important in the
development of individual organisms. This causes them to be increasingly conservative in evolution, and
this together with the inheritance of features down taxonomic lineages leads them to become taxonomic
generalities of increasing scope, broadly represented across many organic types.10
I would prefer phylogenetic commonalities in place of taxonomic generalities,

since the inference is that a generative entrenchment of a radially symmetrical body
form, for example, remains a common feature of the organisms that arise from the
archetype. Some entrenched qualities are universal, such as the relationship between
mitochondria and their eukaryotic hosts. Similarly, chloroplasts are entrenched in
plants. Symbioses are polyphyletic. However, although they have neither taxonomic
nor phylogenetic general significance, the principle of generative entrenchment as
stated by Wimsatt can still be followed. For example, bivalve sulfur-oxidizing
symbioses led to an interdependency between cells with many mitochondria, and cells
containing the new symbionts, and it also had epigenetic downstream effects on the
form of the ctenidia that contain the bacteriocytes, as well as ventilation behavior
(Reid 1990). Yet it also freed many of the symbiotic hosts from the trouble of
developing digestive tracts, and so generative entrenchment does not imply
permanent fixation of all the systems that were interdependent when the entrench-
ment occurred. Some could be free to regress, or to undergo exaptation.
Wimsatt (1999) also makes a necessary distinction between canalization and
generative entrenchment. Canalization is the degree of regulation of developmental
342 Chapter 9
pathways that are epigenetically downstream from the entrenched systems. It is

therefore a sometimes advantageous concomitant of generative entrenchment, but
not the same as generative entrenchment. Once essential interdependencies have
been entrenched they are further stabilized by the syndrome of internal selection, as
L. L. Whyte (1965) proposed. I alternatively use the term co-adaptation for the
internal adjustments that are made in the wake of disequilibrating physiogeneses and
symbiogeneses.
Although we do not yet fully understand how they can be overcome, mechanisms
that accommodate change clearly exist. Homeorhesis is nothing more than the whole
package of accommodatory mechanisms that determines trueness to type in tightly
canalized organisms. In loosely canalized epigenesis, interferences are accommodated
so that the changed product of development is still functionally integrated. For
example, the elongation of one toe in the horse lineage, at whatever stage in its
evolution, could function in locomotion since it was always fully integrated with the
other bones and neuromuscular features of the leg. This would still be true if the
elongation involved a saltatory growth spurt instead of the imperceptible steps
demanded by selectionism. As Goodwin says, this developmental robustness could not
exist if the causes of epigenesis were nothing but the actions of structural genes and
their genomic switches. And as Schmalhausen said, long before, physiological adapt-
ability also accommodates developmental change.
Many progressive epigenetic novelties are critical-point emergences, and can be
explained in terms of constrained pathways, codon or gene amplification, and
repetitive differentiation, the latter fitting Mllers category of secondary by-
products. Internal selection might constantly tighten canalization to the point where
every optional pathway is constrained. However, there is always room for experimen-
tation with redundant DNA, especially if the pool of non-transcribing repetitive
microsatellite sequences is routinely tapped to patch broken chromatid strands,
without interfering with the prevailing dynamic stability.11 The range of such natural
experimental methods is outlined in chapter 6. If the experiments are disintegrative
they will be lost before they are found. If they are encumbrances, such as energy
drains, their persistence will be diminished. When they become manifest in the
phenotype they will be ignored if neutral, and preserved only in the narrow lineage in
which they originate. If beneficial in some way, they will be incorporated into a new
dynamic equilibrium and spread throughout the breeding population. Even if the
innovations are advantageous, their subsequent enhancement may come from an
autonomous, self-amplifying genetic drive, not the approval of selection. Allometric
hopeful monsters are common, even in tightly canalized types. Their evolution is
much easier to understand if they have been autonomously driven through the
incipient experimental phase before they show any kind of advantage. DNA made
redundant by the regression of ancestral pathways of development, along with
repetitive gene and genome amplification and differentiation is a wellspring of exper-

imental material and a key to understanding epigenetic plasticity. Epigenetically active
hormones and enzymes that arise by repetitive differentiation may extend develop-
mental pathways or cause them to diversify by branching.
As Ryuichi Matsuda (1987) proposed, novel environmental influences are also
important for epigenetic emergences. Also, their subsequent internalization into
homeorhesis, as envisaged by Schmalhausen, could largely be explained as genetic
assimilationor epigenetic assimilation. This makes the canalization more
independent of environmental vicissitudes, and establishes a new level of dynamic
stability adjusted to the emergent novelty. Direct environmental effects may also be
exaggerated temporarily by the effects of natural disasters. As well as allowing earlier
emergences to escape from natural selection, catastrophes could conceivably cause
direct changes through extreme physicochemical stress, such as heat shock.
Although the significance of intermediate structures raised by Mller was
anticipated by Riedl (1978) and Matsuda (1987), Eugene Balons development of the
idea in 1986 is the most thorough:
Life processes use bifurcations to create novelties and alternative answers, as and when required
at any interval of ontogeny and evolution. . . . The saltatory mechanisms of epigenesis are
responsible for a sequence of homeorhetic steps that are separated by relatively unstable
thresholds, and . . . during those thresholds changes in life history as well as novelty are
created.12
Balon agrees that there is a tendency toward tighter canalization (and, implicitly,
generative entrenchment) as well as specialization during the course of evolution, but
his research on fish indicates a number of possible escape routes at epigenetic
thresholds, some of which are marked by larval and juvenile behavior changes during
normal development. An external or internal environmental change at a threshold
can result in a variant phase of development that may be effected by allometric shift
or another epigenetic accommodation. An interesting case is that of Arctic char that
are ice-locked as juveniles. At the stage of development when they are ready to forage
for themselves they have no access to the atmosphere for filling their swim bladders.
But they compensate by developing lighter skeletons than conspecifics who can more
typically swallow air at the appropriate time.13 Large eggs buffer development through
the early thresholds, and so offer greater homeorhetic stability as they head toward
their established specialization. However, a sheltered childhood is not bound to have
such an effect. In mammals, for example, it has a distinct advantage before adult phys-
iological homeostasis stabilizes. But that has not prevented anatomical diversification.
Developmental arrest and paedomorphosis are common regressions that sometimes
follow through to bigger and better things, while leaving clues to their historical
occurrence. For example, in hominid evolution, juvenile anatomy is prominent, while
hypermorphosis increases brain size, and adjusts bipedalism, a vertical stance, and
344 Chapter 9
vocalization. In any case, Balons and Mllers point is takendiscontinuous phases in

development present opportunities for emergent evolutionary change. This is a nice
fit with John Hollands concept of a transition function whereby a change of state
allows several different strategies to operate.
It is appropriate to return here to the epigenetic influence of symbionts. The
presence of nitrogen-fixing bacteria in host plants stimulates nodule formation, and I
suspect that sulfur-oxidizing bacteria and dinoflagellate symbionts may also have had
epigenetic effects on their hosts. The ability of retroviruses to be transmitted as
oncogenes that locally disinhibit cell division, resulting in tumors, though
detrimental in this case, is in the same category. Hypothetically, retroviral transgene-
ses could have beneficial, epigenetic effects. According to the human genome project,
numerous transfers of genes from bacteria have occurred relatively recently, some of
them with advantageous qualities. There is also growing evidence that gut microflora
affect development of the alimentary tract. In humans, some relatively benign
parasites such as pinworms trigger the development of defense mechanisms that
prevent more serious ailments later in life. As I noted in Evolution by Association,
gut bacteria also effect normal gut development and digestive and immunological
functions in mice. Just as interesting are the free-living bacteria that stimulate the sea
lettuce, Ulva, to make lettuce-leaf thalli instead of the thready form that they have
in axenic (sterile) culture.14 Nitrogen-fixing bacteria stimulate the formation of root
nodules in their host plants. Brian Hall (1992) classes these kinds of influences under
interspecific epigenetics. We should also recall intraspecific effects such as alterations
in feeding regimes that differentiate castes in ants and termites.15 There are also the
consequences of overcrowding that change locust color and behavior, and that
produce monstrous carnivores among salamanders. These changes overlap with the
physiological factors.
Body Plans
The diversification of body plans among multicellular animals has been addressed
by a number of authors, especially during the last decade. It is a subject that I have
not elaborated. However, the notion of a single body plan common to all multicellu-
lar animals has an unavoidable theoretical allure. In The Plausibility of Life (2005),
Marc Kirschner and John Gerhart propose that such a universal body plan has existed
since the late Pre-Cambrian, though expressed in evolution in a number of diverse
forms. It usually occurs in a bilaterally symmetrical organism that in its simplest state
consists of a series of compartments, not necessarily visible, as in the case
of segments in annelids and arthropods, or serially paired somites in vertebrates.
The compartments are semi-autonomous regions whose forms and functions are
regulated by differentially expressed Hox genes (not to mention many others,
including Wnt). They constitute an invisible map that has no simple anatomical
equivalent, since the compartments cooperate locally to produce visible morphologi-
cal features, such as segments and limbs. The diversity of body forms, whose differences
we tend to emphasize when we examine them, is thus the product of differential
regulatory gene expressionto which we must, of course, add the effects of the
external environment, the overall behavior and physiology or the organism, and
related genomic changes.
The Big Top
The circus is an adequate metaphor for the complexity of the structures and functions
of the biosphere. We can concentrate on the performances in a particular ring, or sit
far enough back to view all three rings and take in the aerialists under the big top. It
is complex, and dynamic, and the ringmaster is trying to keep it under control. He
cant keep his eye all the time on what the clownsthe generalistsare up to as they
fool around with new acts in obscure corners, nor can we. Because it is mostly in a
state of dynamic equilibrium, the circus metaphor has its limitations. To view
progressive movements in evolution we need to look at the bootstrapping relation-
ships between development, physiology, behavior, association, and environment, as
well as their hierarchical structures.
Curiously enough, in view of the claim of the Modern Synthesis to synthesize
ecology and genetics, there is no existent theory of environment of much value to
emergentism. Environmental biology comes in bits and pieces, and are assumed to be
integrated under selection theory. But theories of demographics take environment too
much for granted. In the context of adaptation by natural selection, environment is a
mere backdrop to the real action, or a bag for the gene beans. Richard Lewontin
provides a thoughtful epigraph for this section:
Just as there is no organism without an environment, there can be no environment without an

organism. . . . An environment is something that surrounds or encloses, but for there to be a
surrounding there has to be something at the center to be surrounded.16
Lewontin writes in The Triple Helix (2000) that Darwins role in separating the
organism and its environment was a necessary step for the analysis of natural selection
and population studies and ultimately molecular biology. And he rightly argues that
it is now time to put them back together again. We shouldnt be too hard on Darwin;
he knew that the bank was tangled, that populations of cats and mice and bumblebees
were related, and that the earthworm, perfect in its adaptation, had a massive
ecological impact. His greater sin was in separating the organism from its development
and physiology, turning it into an abstracted pawn, to be sacrificed or crowned
according to time, chance, and natural selection.
346 Chapter 9
One of the subjects of Lewontins critique is the Darwinist idea that an environmen-
tal niche can exist in anticipation of an organisms occupation of it. As its proponents
might say, the environment constrains and pressures the organism into a particular
adaptational direction. Yet, as Lewontin points out, we can identify many such
potential niches that have never been occupied. And I have already provided examples
of potential adaptations that would require only the slightest nudge to pre-existent
qualities. But the slightest nudge is still not a real force. Lewontin notes that birds that
nest in trees do not eat the foliage of the trees. Maybe the hoatzin is an exception,
since it can eat and digest foliage due to its cellulolytic symbionts. But it prefers juicy,
low-growing marsh plants. In any case, most birds that dwell in trees do not eat the
most abundant source of potential food. My daughter Clio has worked with the
kakapo, an endangered species of flightless parrot, endemic to New Zealand, whose
population numbers less than 100.17 A ground-nesting bird, it climbs trees to find fruit
and seeds, and to roost. Its large size and relative inability to escape introduced
predators, has brought it close to the fate of the similar dodo. Like the dodo, and other
extinct flightless birds, it has done nothing constructive with its wings. It hasnt
turned them into hands. It doesnt even use them to hold on when it climbs. At best
it seems to use them as stabilizers when they jump or fall out of their trees. Hand-
reared young wave their wings in apparent approval of human helpers bearing gifts of
foodor to slap them in the face when they err in their ways. So there is a possibility
that they have some secondary sexual signaling function during matingwhich has
not at the time of writing been directly observed. There are all kinds of potential
niches beckoning to flightless birds with hands, but they have ignored the invitations
to exapt. Why-not questions are interesting, but philosophically illegitimate.
Therefore, we will not explore the significance of entrenched generative systems and
epigenetically constrained pathways in this regard.
As J. Scott Turner (2000) remarks, the early ecological theorists Whitehead,
Clements, Tansley, Hutchinson, and Odum had roots in holism, and they did not
draw a distinct boundary between the organism and its environment:
Presently, biology that is not strictly materialist or reductionist is commonly regarded as

somehow suspect or deficient in intellectual rigor. Even among ecologists, I think it fair to say,
good ecology is defined by the distance one can put between it and the holistic philosophical
leanings of the early ecologists.18
As a physiologist, Turner can understand that point of view without sympathizing

with it. Physiologists only temporarily reduce systems to their parts before putting
them back together again, and Turner goes further than most physiologists in
restoring the organism to its environment (q.v. below). In my own case I can hardly
listen to an ecologist say Im a reductionist and proud of it without registering my
disbelief.
An environmental theory necessary for an emergence synthesis would look similar

to a blend of Lamarckism and neo-Lamarckism, without the inheritance of acquired
characteristics. Although Lamarck believed that the natural course of evolution was a
gradual, intrinsic increase in complexity and organization, he knew that it was
changed by ecological encounters:
. . . by the influence of circumstances upon habits and then by habits on the state of the parts
and even on organization, each animal can receive in its parts and its organization modifications
susceptible of becoming quite considerable and of having given rise to the state in which we now
see all the animals.19
Environment pervades the developmental, physiological and associative theories that

I have just discussed, yet its importance demands an independent section of this
chapter. In this instance I will follow a hierarchical approach from molecule to
biosphere.
The Molecular Environment

The realization of genetic information depends on multiple factors, among which are
the absence of repressors, presence of inducers, association with binding proteins and
form-making proteins (prions and stress proteins such as chaperonins). Local ionic,
electric, hydrophilic, or hydrofuge conditions, and organelle compartments, are also
affective. The principle of homeostasis can be applied at this basement level, to
explain how things stay the way they are: evolutionary experiments are blocked, and
molecular glitches repaired. Change in these conditions can effect evolutionary
change, and lift the lid of the molecular alchemical cauldron enough to let the
occasional experiment escape. Weng et al (1999) have shown how the contingent
association of biochemical pathways, and the use of molecular scaffolding to channel
reactions and improve their efficiency, can all generate a tremendous range of novel
properties. There is such great potential that the number of emergences is not an issue,
but constraining them epigenetically and inhibiting them into ordered activity is.
Homeotic gene mutations can produce saltatory epigenetic change when they get
away with it. Experimentation is enhanced by the availability of spare parts through
codon, exon, gene, and genome duplication, as well as the shuffling of exons, introns,
and protein domains.
The Cellular Environment

Here we go outside the cell to the internal milieu, so that we can consider how cells
are affected by that environment and intercommunicate through it. In varying
degrees, cells influence each others mitotic cycles and differentiation. The fluid in
which they are bathed is under homeostatic regulation, but change in local conditions
allows escape from sameness. Differential adhesion of cells can affect organismal form
348 Chapter 9
through changes in self-assembly, even before genetic assimilation brings genes into
play. The orientation of sheets of cultured cells has been shown to respond to light
signals, and there is a faint possibility that photon emissions from metabolic processes
can be detected by adjacent tissues.20 Light stimulation is known to be important in
the development of cells and organs that use light as a source of energy or
information. Migratory mesenchyme cells can experiment with the redistribution of
tissues. Neural crest cells can alter major patterns of development of vertebrates. Cells
such as neurons that grow probing and communicating axons can be powerful
epigenetic inducers. Even more striking is the way in which they intercommunicate to
generate evolutionary and ontogenic emergences that we call memory, intelligence,
logic, language, consciousness, aestheticsand, taking them together, mind. Koch and
Laurent (1999) demonstrate that on top of the intracellular signaling potential of
neurons, the emergent combinatorial potential of multiple dendrites, and intercellu-
lar signaling molecules is enormous. This emphasizes the conclusion reached by
Wimsatt (1997) to the effect that once mere aggregates have been removed from con-
sideration, the possibilities for emergent changes to wholes that are greater than the
sums of their parts, both physical and biological, are almost infinite. Endosymbioses
and other interspecific cellular relationships allow a nutritional mutualism between
host and symbiont cells that is a significant emergent property. Furthermore,
endosymbioses influence the epigenesis of the host.
The Organism and Its External Environment

Compared to the way in which the biotic, intraorganismal environment can be com-
plexified by the endogenous activities of cells, the physicochemical effects of the
external environment are simple, but nevertheless significant. They impose
themselves on the internal milieu of primitive organisms. They may impose stresses
that alter heat-stress protein functions and methylation patterns. Therefore, wherever
their behavior takes organisms, both molecules and cells are affected, in their
development and physiological function. Major evolutionary changes have been
initiated by non-heritable influences of the external environment. Physical factors
include light, temperature, high-energy radiation, diffusion, osmosis, gravity,
electricity, electromagnetic fields, surface tension, friction, and mechanical stress.
Chemical factors include the concentrations and proportions of ions, nutrients and
the properties of colloids. Biotic factors include symbionts, conspecifics, other
organisms, and airborne or water-borne biochemical messenger molecules. These may
have direct influences on development, physiology and behavior, through sexual
reproduction, the establishment of new symbioses and other associations,
competition, disease, predation, or browsing. The more adaptable the organism, the
more it can experiment with behavior and explore new environments. By consistently
and persistently responding to a particular environment in a particular way an
organism can direct the future of its lineage toward particular functional and
anatomical adaptations.
I have already touched on the larger aspects of geophysiology that have wrought
diversions in the course of evolution. They have also contributed to Gaian
homeostasis, to which I will return to it in the section below on the biosphere.
Organisms can also effect small changes in the local environment that might be
beneficial to them directly, or through consequent changes in local community
structure. These local changes make up much of the substance of J. Scott Turners The
Extended Organism (2000). He justifiably makes much of nest building and burrowing
as habits that make environments less stressful, and often more productive of
potential food organisms. I have a personal stake in such matters, having studied
burrowing benthic marine animals for all of my career, and know how oxygenation
and the consequent changes in bacterial communities can enrich the sediments. Such
processes can be intermediaries in the invasion of hostile environments. Soil building
by primitive plants is also a local effect with a global consequence.
In rising through the hierarchical biological levels we come to populations and
species. As populations expand in numbers and space they will encounter and be
limited by stressful conditions. The most adaptable members of populations will be
most likely to endure at the edge of chaos, trading off physiological stress for limited
competition. They are not so much selected by the environment as self-selecting for
the environment. Those that possess the appropriate emergent qualities can penetrate
environmental interfaces to found new lineages that are genetically and epigenetically
different from the parental population. They do not need to pass immigration
inspection to do so. Since this is close enough to the conventional allopatric model I
will not further expound it, except to say that large numbers of individuals might be
capable of simultaneously penetrating the new environment. Thus, the emergent
qualities of the new population are features that already existed at the interface, they
are common to all of the new immigrants, and not the consequence of new strong
selection pressures.
The catalysis of stress is not limited to environmental boundaries. Overpopulation
can stimulate some profound epigenetic changes. The example of the emergence of
carnivorous monster salamanders that reduce the numbers of the normal vegetarian
type is a case in point. Overcrowded locust hoppers are epigenetically stimulated to
become flyers. During the evolution of these phenomena there might have been an
initial selection for the flyers. But who is to say that their departure did not restore
the parental population to its carrying capacity and so continued survival. One thing
is sure, the novel deme that flew to pastures new was entirely composed of individuals
who had the epigenetic plasticity to fly when the environment told them to.
Thus, stable phases and turbulent thresholds exist not only at the developmental
and physiological and behavioral levels, they can also be detected at the population
350 Chapter 9
level. An awareness of this is to be found in Mivarts intermittent stable equilibria of

organismal evolution, and in Eldredge and Goulds initial exposition of punctuated
equilibria of speciation.
The Biosphere
The word biosphere was coined by Austrian geologist Eduard Suess in 1875, and the
concept was developed by Vladimir Vernadsky in Biosfera (1926). Vernadsky saw it as
a heterogeneous sphere of living matter, which he sometimes called animated water
since it was largely in and of the hydrosphere. The animated water of microscopic
unicells, plants, and fungi continued from the seas and lakes onto the land. The
biosphere was also in dynamic equilibrium with the lower geological substratum, and
with the atmosphere. Beyond it lay an outer sphere of cosmic energy that came mainly
from the sun. Before the 1998 publication of Vernadskys book in English as The
Biosphere, James Lovelock (1979, 1988) had proposed his Gaia theory, which included
the evolution (sensu lato) of the biosphere. He also recounted the development of
Gaia, with well-argued details regarding atmospheric oxygenation, albedo effect, the
climatic and nutrient roles of sulfur compounds, and other ways in which organisms
interact with their environment. Lovelocks mechanistically objective explanations
more than compensate for what some of his readers find too metaphysical or even
mystical. Like Vernadsky, Lovelock appreciates the feedback between organism and
environment on a large scale, and like James Hutton (1785) sees that there is a geo-
physiology analogous to organismal homeostasis.21 Hutton, a physician and an
agrarian by training and experience, was also a theoretical geologist. His correspon-
dent Erasmus Darwin also saw animal physiology as a model for both organization
and evolution of the Earth.22 Lovelocks sometime collaborator Lynn Margulis has
properly added symbiosis as a crucial emergent property of the biosphere.
In a variety of ways, organisms can alter the biosphere locally and temporarily.
Effects such as epidemics, population explosions of pests, parasites, and predators can
seem devastating from the human perspective. Less dramatic alterations of soil
building on land, and eutrophication of lakes and seas are, however, more important.
Sudden rises of redox layers in aquatic environments can cause die-offs that increase
biological oxygen demand and allow sulfide buildup. Instead of being decomposed
back to carbon dioxide and water, organic debris might be partly sequestered, and
fossilized, without consuming oxygen. Ecosystems, and patterns of climate can be
altered by the evolution and redistribution of plants. Several symbioses have played
major roles in such changes, though none can match the oxygenation of the
atmosphere by symbiotic photosynthesizers.
Large-scale changes have led to the biosphere with which we are familiar. But the
dynamic stabilities of Gaia have not followed the same path as biological homeostasis.
Although they involve some physicochemical stability through negative feedback,
they have not advanced to a state of sophisticated resistance to change. That is just as
well for biological evolution, which has needed the capricious clean sweeps of electro-
magnetic reversals, plate tectonics, volcanic activity, glaciation, deluges, sea-level
changes, and the impact of comets and asteroids. These environmental alterations
were part of the substrate of progressive emergent evolution.
In progressing from molecules to the biosphere, we have taken one aspect of the
environment so much for granted as to ignore it. Therefore, lets go back to
Vernadskys idea of animated water. We inhabit a planet where water is usually in a
liquid phase that possesses anomalous physicochemical qualities. Life in all its mani-
festations would be impossible without the emergent wetness of H2O. Water is not
only the universal solvent of the internal and external milieux. It buffers temperature
change in all of its standing bodies, from puddles to oceans. My colleague Richard
Ring found that a beetle, Pytho deplanatus, survives supercooling to 54C because it
accumulates the antifreezes glycerol and trehalose in its body fluids.23 At the other end
of the temperature range, water, under sufficient pressure, remains liquid to its critical
point of +374C and 3,212 pounds per square inch. This makes it more plausible that
life might have originated at high temperatures deep in the Earths crust. Water is a
reactant in a wide range of biochemical processes, and its kinetic properties are partic-
ularly important in calcium-mediated functions. It is also a structural component of
proteins, cartilage, and bone. Water is the medium of blood circulation; it cools by
surface evaporation; its hydraulic behavior affects growth and moulting in
crustaceans, locomotion in small insects, spiders, octopuses, slugs, snails, earthworms,
and echinoderms. Under pressure, it also affects excretion in kidneys, feeding behavior
in carnivorous clams, metamorphosis in insects, the epigenesis of eyes and brains, and
sexual intercourse.
At the surfaces of bodies of water, where the temperature falls below 0C, its
supramolecular structure and cohesive properties are capable of change, yet it does not
immediately crystallize to ice without physical stimulation in the form of nucleating
agents or mechanical disturbance. Its cohesiveness increases at biological surfaces, and
it presents different fluid-dynamic challenges to microscopic and macroscopic
creatures. There is no gene for water, any more than there are specific genes for
particular behaviors. Yet, as much as behavior, water molded the early evolution of
function and form. Then, when organisms emerged from water, they carried it in their
internal milieu. And its very absence from the terrestrial environment molded them
even more.
Processes of Natural Experimentation and Their Emergent Results
Now that the various causal arenas have been surveyed, it can be asked what processes
and mechanisms of natural experiment and emergence are common to them all? The
352 Chapter 9
answers can be cross-referred to hierarchical levels. This may bring us closer to a

unifying synthesis of emergence, or demonstrate that such a unification is impossible.
Darwins entangled bank microcosm of biotic complexity was a product of
Growth with Reproduction; Inheritance which is almost implied by Reproduction;
variability from the indirect and direct action of the external conditions of life, and
from use and disuse; a ratio of increase so high as to lead to a Struggle for Life, and as
a consequence to Natural Selection, entailing Divergence of character and the
Extinction of less-improved forms.24
Darwin was comprehensive enough for his time, especially after he co-opted neo-
Lamarckism. And he had his priorities in the right order too, except that divergence
of character is also prior to the consequence of natural selection. But what
mechanisms and processes raise emergences from their generative foundations? Some
answers have already been provided, especially in the Where Are We? section at the
end of chapter 7 and in the introduction to the present chapter, but they bear
elaboration. I begin with the simple process of reproduction that characterized the
emergence of life, and then those mechanisms that emerged from simple reproduction
to generate greater complexity and persistence in being.
Organismal Reproduction
Duplication of the whole organism requires duplication of the genome. In most
sexually reproducing organisms a haploid copy of the genome is contained in an
appropriately structured gamete. Of the gametes, the egg cell is most important to the
developing embryo, since it provides a suitable milieu, molecular resources, and
organelles. It also initiates a chronological series of epigenetic triggers not all of which
are genetic. The size, structure, and constituents of the egg are crucial, as are environ-
mental stimuli. Since the integrity of individual organisms eventually fails by time and
by chance, reproduction ensures the continuity of life. It therefore generates persistent
complex patterns on a scale quantitatively and qualitatively different from non-living
systems. Starting from scratch in every generation from a single cell also exposes every
organism to epigenetic experiment.
Because of the inherently experimental nature of the copying process, biological
reproduction and duplication of the constituent holons of the organism have the
emergent potential for differentiation. But to reproduce, individuals must first survive,
and that depends upon their integrity, the improvement of which is the mark of
progressive evolution. Sexual reproduction was a novel experiment consisting of an
emergent combination of genome duplication together with an intimate association
of partners or their reproductive products. Even excluding gene duplication and
mutation, it made possible repetitive differentiation at the genome level, and that
allowed much greater freedom of experiment with phenotypic variability, while
retaining sufficient reproductive faithfulness that the novelty would not be lost to
subsequent generations of the lineage in which it occurred.
Progressive Homeostasis
The ability to persist in being was one of the first organisms fundamental character-
istics that made evolution possible as soon as they emerged. Along with reproduction,
self-maintenance was a sine qua non of evolvability, and the complexification of
homeostasis was a major part of progressive evolution in animals, and in plants too,
though the concepts differ somewhat. Many of the following mechanisms or processes
have contributed to one of the most fundamental features of animal progressive
evolution; i.e., the possession of an internal milieu that supports increased behavioral
flexibility and freedom of choice. The early stages of this physiological evolution
depended upon a bootstrapping process of feedback between behavior, environment,
the physiological state, and development. Once the homeothermic condition was
locked in as the final step in physicochemical homeostasis, it was possible to generate
a metabolic rate necessary for sustaining a sophisticated nervous system, and conse-
quently intelligent behavior. The placental mammal is the only type whose
homeostasis is consistent throughout the entire life cycle. At this stage physiological
homeostasis is the major generative condition of further evolutionary advances in
behavior, anatomy, and association.
This process of improvement of the organisms integrity operates in every causal arena
of evolution as a mechanism of overall enlargement, allometric shift, and the
provision of differentiated units that can ultimately be coordinated in a complex
hierarchy. While the mechanisms vary in the organismal hierarchy from the
molecular to the social it amounts to a common process that constitutes a general
principle of emergence that operates in space and time.
At the biochemical level, repetitive differentiation of DNA produced gene families
and hence multiple homologues of structural proteins and enzymes, permitting the
buildup of biochemical pathways and cycles. As a result, different enzymes and
hormones based on the same ur-DNA could provide for greater physiological adapt-
ability, making even primitive organisms less vulnerable to the vicissitudes of
environmental change. The mixing and matching of protein domains led to even
more dramatic biochemical emergences. However, the number of protein domains is
fewer than the total number of genes, since the polypeptide backbone and amino acid
side chains have a constrained geometry. The same limitation applies to domain
mixing and matching.25
At the organ level repetitive differentiation of anatomical units allowed
the separation and concurrence of physiological offices. This was enhanced by
progressive packaging, which also improved the organization of rapidly expanding
tissues such as the neocortex of the brain. Even after the brain functions have become
relatively fixed, differentiation of integration, in the form of rewiring, have produced
354 Chapter 9
evolutionary change. And novel dendritic connections have both phylogenetic and
ontogenetic qualities.
Multicellularity potentiated all of the epigenetic differentiations that built upon one
another to construct the complexity of plant and animal life. This exposes the
arbitrary nature of separating evolutionary causes into three arenas. Though
convenient for simplicity of analysis, they cannot be left so disjointed. Physiological
progress and anatomical diversification would not have happened in the absence of
evolving multicellularity.
Social associations among insects are analogous to repetitive differentiation of
multiple cells: specialized castes come from repeated organismal units. Finally, family
and social groups in higher animals emerged from generative conditions provided by
epigenetic and physiological advances in neural self-organization. And, within large
social groups, behavioral specialization could arise without commitment to genetic
fixation.
The evolutionary significance of repetitive differentiation as varied repeats has
finally been appreciated by molecular biologists. The concept illustrates how natural
experiments can take place out of sight of natural selection, and how the simplest kind
of self-replicating system can spontaneously become complex and potentially self-
organizing through multiple feedback controls. And it applies to the duplication of
discrete codons, exons, introns, genes, chromosomes, karyotypes, cells, tissues,
organs, segments, organisms, populations, and societies. The principle also embraces
wholes that are greater than the sums of their parts, but also implies that they can
progress to higher levels of complexity and wholeness.
Repetitive differentiation also provides redundancy, which also fits the metaphor of
evolution by natural experiment. Spare partsgenes, organelles, organs, clones,
asexual organisms (in societies)might be duplicates of those with essential
functions. Or they may simply have become redundant because the original role is no
longer necessary and thus freed to do something different. Therefore, Dohrns func-
tionswechsel and Gould and Vrbas exaptation are relevant to this kind of natural
experiment.26
Mixing and Matching

As soon as molecular, cellular, organ, and organismic holons began to be repeated and
differentiated there was a wealth of material for experimental mixing and matching.
At the genetic level Von Uexklls piano metaphor applies: the same set of keys can be
played in a simple linear series as a scale, or in a huge variety of chords and tempos to
become a concerto. If we were to take protein domains as the keys the keyboard would
be very simple. If modifier genes as well as structural genes are taken as equivalent to
the piano keys, many varieties of epigenesis are achievable. If the differentiating
process involves the mixing and matching of exons, to produce biochemical novelty,
the possibilities increase greatly, though the final products in the form of novel
proteins are constrained as noted above. Intragenic shuffling of the existing pack of
genes can also introduce some novel combinations, but the list of known examples
remains quite brief.
During epigenesis, mixing and matching of cells that influence development have
been involved both in homeorhesis and in experimentation with epigenetic novelty.
Implicit in genetic and epigenetic combinations is a canalizing algorithm that usually
makes the organism true to type, but occasionally changes to produce experimental
forms.
At the organism level, mixing and matching of symbiotic proto-bionts, prokaryotes
and eukaryotes have produced new types, sometimes with sufficient impact to found
new ecosystems. By the same principle, at the ecosystem level, communities, and
more intimate co-evolutionary relationships have emerged.
The Acquisition of Heritable Characteristics

Gene acquisition from extrinsic sources is a special case of mixing and matching.
Natural transgenesis is so common in prokaryotes it makes phyletic relationships
between their ancient ancestors highly complicated, and guarantees their descendants
resistance to antibiotics. The acquisition of heritable characteristics that was part of
endosymbiosis. was a major advantage to eukaryotes, but at that point their ability to
get genes from foreign sources was greatly diminished. While retroviral gene
acquisition has occurred in eukaryotes, it has not, as far as we yet know, been a major
influence. If the acquisition of transgenes was a primitive source of evolutionary
novelty, it has become redundant in the higher social animals, which depend on intel-
ligence and learning.
Self-Organization
My readers would, I hope, agree that reproduction and self-maintenance were the
fundamental characteristics of life, and that complexifications of those emergent
properties the most central processes of evolution. Conceptually, self-organization
could be equated with self-maintenance in the most primitive organisms. But as soon
as something like a cell cycle emerged, self-organization became a distinctive feature
that was also subject to emergent evolution. With the emergence of multicellular
organisms, self-organization from a single cell, or small number of cells, to a differen-
tiated condition became one of the most visible modes of evolution, most strongly
linked with epigenetics. The following categories of evolutionary process are subsets
of this one.
Heterochrony
Once the foundations of the structural genome were in place, and the switching
mechanisms of the epigenome and its associated regulatory proteins wired in, there
356 Chapter 9
still remained a considerable degree of adjustability for the final form of the organism
through the chronological rearrangement of switching, and consequent alteration of
expression of the structural genes. Any organism that changes during its life cycle,
including a prokaryote, is subject to the effects of the passage of time, and to
associated intrinsic and extrinsic changes. Therefore, heterochronous changes are
virtually universal natural experiments in evolution. Like Bateson, Goldschmidt, and
Riedl, we might find it difficult to conceive of a complex organism changing at its
lower hierarchical levels without destroying the upper ones. But we can evade Fishers
total denial of the possibility by perceiving that complexification occurs in the
dimension of time, and enjoys the pre-existent adaptability of the organism. In other
words, the individual has the opportunity to respond appropriately throughout its
development. Thus, in addition to recombinant variability, sexual reproduction has
imposed development from a fertilized egg on every generationproviding for evolv-
ability.
Some timing alterations in development are made possible by repetitive differentia-
tion. More proteins, for both construction and function, can increase rate of growth
and more ribosomal RNA can get developmental processes off to a faster start.
Heterochrony is also effected by environmental change, and the trigger can become
internalized in epigenesis to result in greater homeorhesis.
Allometry and Orthogenesis

This could be regarded as a category of heterochrony, with strong causal links with
repetitive differentiation as set out above. Some molecular events increase the
likelihood of recurrence in future generations, thus constituting a kind of mechanistic
drive. These include codon amplification through DNA replication slippage, gene
duplication, concerted evolution and dosage amplification, resulting from unequal
recombination, and corollary mechanisms provided by recombination enzymes and
jumping genes. Along with redistribution of cells that affect epigenesis, these
contribute to allometric growth changes, phenomena that used to be collectively
called orthogenesis. Many instances of evolution by so-called directional selection
are probably manifestations of allometric shifts caused by epigenetic drives, or by
epigenetic constraints that allow change only along a single pathway. Orthogenesis is
not a random process subjected to natural selection, so it can be carried to the point
of ultramorphosis and extinction, since all the members of the phyletic lineage that
possess it are driven in the same direction. But most known cases of allometric shift in
the lineages of surviving organisms stopped before they went that far.
Orthogenesis fits the category of an autonomous critical-point emergence, although
it may proceed rapidly enough to appear to be saltatory. If it is adaptively neutral, the
lineage in which it occurs will continue to possess it, and the gene and protein family
will continue to be driven to further multiplication. This is the most interesting case,
since it solves the problem exposed by Mivart, and worried over by Darwin, about the
absence of adaptiveness in the incipient stages of evolution of complex functional
anatomies. There is no question about the reality of this phenomenon or about its sig-
nificance for anatomical diversification. Orthogenesis to ultramorphosis and
extinction is a possible outcome, but most of the instances of allometric growth with
which we are familiar stopped before the terminal stage of exaggeration was reached.
Penetration of New Environments

Another very general rule is the origin of novelty at the edge of chaos, or, more
explicitly, under unstable conditions. The mechanisms vary, but the principle is the
same. Innovatively adaptable organisms emerge at stressful environmental interfaces
to penetrate into new conditions of life. Epigenetic innovations emerge at develop-
mental thresholds after periods of stable growth. Some organisms that congregate at
environmental fringes or interfaces may interact epigenetically or symbiotically.
Populations expand in a stable manner until internal overcrowding or physicochemi-
cal limitations at the boundaries disequilibrate them. As a consequence,
physiologically and behaviorally adaptable organisms may individually or en masse
remove themselves to new environments. Speciation is a subsequent event.
A variety of names have been applied to the rule that has just been outlined.
Mivarts intermitting conditions of stable equilibrium would have logically covered
all of the implications, including saltation. Punctuated equilibrium is more succinct
as well as more familiar. At a time when a speciation event was considered a pivotal
evolutionary occurrence, Eldredge and Gould applied punctuated equilibrium to the
relatively sudden origin of species. But the term has a more general theoretical
potential that I will apply unless the proprietors object.
Once new environments have been penetrated by adaptable organisms, they are
more free to experiment with new developmental patterns, and exploratory behaviors
that might not simply lead to physiological modifications, but also diversifying, adap-
tational evolution. This recourses back to heterochrony, repetitive differentiation,
allometry/orthogenesis, and also links with the following.
Genetic Assimilation
Being simply the contingent imposition of physicochemical change in the organism
by the environment, physiogenesis affects generative conditions, but is not a tool or
mechanism of evolution. The genetic assimilation of such change is. As a general
principle, internal adaptation of enzymes and organs to prevailing physicochemical
conditions limits the survivability of an organism if those conditions are susceptible
to change. But general adaptability to respond to environmental change finally
produces an effective homeostasis that subsequently remains stable and persistent.
Genetic assimilation begins with the internalization of contingent changes. Instead of
358 Chapter 9
being susceptible to an environmental cue for an epigenetic event, the organism

produces its own trigger, which may be gene-based and thus may persist as an
epigenetic mechanism. The ostrich, for example, develops appropriate calluses prior to
frictional contact with the ground. Or if a dormant gene can be advantageously turned
on by a drastic temperature change, variants of the gene that turn on spontaneously
might have greater survival potential. The appearance of new genes through exon
shuffling and tandem repeats, together with new proteins through domain mixing
might significantly increase such adaptations and adaptabilities. But emphasis on
gene contribution to genetic accommodation oversimplifies something that must
involve the modification of existent mechanisms of epigenetics, physiology and
behavior. The principle of genetic accommodation addresses how flexible behavior
can become stereotyped. How then does an organism escape its instincts and progress
to freedom of behavioral choice? The answer would seem to be an allometric
expansion and reintegration of whatever parts of the nervous system can override the
gene-determined behavior. Fundamentally, the organism does not, through natural
selection, evolve solutions to problems set by the environment. The organism
determines what is adaptive through its behavior, which is in turn substantiated by its
physiology.
Phase Transitions
At the beginning of this chapter, following the examples of Kauffman (1993) and
Goodwin (1994), I cryptically stated: Where the generative conditions are sufficient,
saltatory emergences may occur spontaneously through self-organizing phase
transitions. The concept is based on a physicochemical model. Under decreasing
temperature an amorphous liquid phase of water will suddenly turn into an ordered
crystalline phase of ice, sometimes speeded up by the presence of nucleating agents.
Under increasing pressure, a colloid gel will go into the sol phase. The idea of such
critical-point phase shifts might seem to apply to emergent evolution. The difference
is that water and gels do not suddenly acquire the ability to change phase. They are
fundamental physical qualities that are immanent in water and colloids.
The same is true of an apparent phase shift from an aggregation of cells to a multi-
cellular organism. It has long been known that if the cells of a sponge or a simple
cnidarian are sifted completely apart they will reassemble themselves into something
like the original animal. Therefore a disordered suspension of cells undergoes a phase
shift into a self-organized organismic entity. But the cells already possessed the ability
and the experience to form themselves into multicellular units. The same is true of the
shift in the slime mold Dictyostelium from the unicellular ameboid phase to the
multicellular fruiting body phase. Intercellular contact is the trigger for an epigenetic
algorithm that already existed. The interesting question is: was the potential for mul-
ticellularity and alterations in cell products initially a non-heritable consequence of
cell contact, which was then genetically assimilated. The simplest multicellular asso-
ciations were sheets and spheres that might have formed with only the simplest of cell
adhesion mechanisms. Once they existed, they must have been sufficiently exposed
to varied environmental factors to autonomously begin differentiating. A biological
model that complexity theorists like is the change in behavior of ants into a more rec-
ognizable rhythmic order when their population density increases to a critical point
that can be defined as x ants per square centimeter, a system mathematically modeled
by Cole (1991). Now, this built-in feature is not evolved anew in every generation of
ants. Was the acquisition of ordered behavior a critical-point emergence at some time
in the ants evolutionary history? The question is answerable through the experimen-
tal manipulation of population densities in the solitary relatives of social insects, and
so is not totally speculative.
The expression phase transition can be metaphorically applied to the threshold
transitions in ontogenic and emergent evolutionary changes of state discussed by
Balon, by Mller and Wagner, and by Holland. But it forces the metaphor too hard to
apply it to cases of critical-point evolution such as the transition from non-flight to
flightwhere no flight had existed before. It is an impressive sight to see a flock of
starlings feeding randomly on the ground, and then take to the air like a superorgan-
ism: phase transition would seem superficially appropriate. But it is inherent in the
nature of starlings, not a novel emergent feature. When flight first evolved it too was
relatively sudden. When allometric growth increased the size of wings there was a
point in the life of individual proto-birds when true flight occurred. But this goes
beyond the point where the metaphor of phase transition has any explanatory value.
When I said that saltatory emergences may occur spontaneously through self-
organizing phase transitions the emphasis is on the autonomous emergence of novel
features, not on the shift to a phase that was already inherent in the physicochemical
generative conditions. I might have been wiser to have avoided the metaphor
altogether, but leave this section intact, since it is such a popular notion, even among
the cognoscenti.
Contingency-Dependent Emergences
If you scan the headings in the previous list of tools and techniques of natural exper-
imentation, you will detect a bias in favor of endogenous or intrinsic mechanisms.
Also important are cases where the action of the organism has a feedback effect from
the environment, and where accidents of nature are also causal. On many occasions
the origin and success of intrinsic emergent novelties, including some of the threshold
conditions frequently referred to above, has depended on such contingencies. Being in
the right place at the right time is particularly apt when random climatic, tectonic, and
catastrophic changes occur. However, physiological and behavioral adaptability is
prime catastrophe insurance, even among the lucky ones. Some external conditions
360 Chapter 9
can be controlled, in the sense that the organism can choose to expose itself to them
or avoid them, such as staying at home in the sea or venturing into fresh water. In
addition, some chemical geophysiological environmental changes, such as the
oxygenation of the biosphere, resulting from the action of emergent organisms,
created new conditions that would affect subsequent evolution.
Contingencies are part of the history of emergent evolution. For example, potential
symbionts that had followed their own independent courses until the moment of
symbiotic truth had to come together for long enough in sufficient numbers to reach
that threshold. They had to be in the same place at the same time. Moreover, they had
to have retained sufficient genetic compatibility since their original divergence from
common ancestry. Modularity of molecular, and cellular structure was also significant
in successful physiological emergences.
Disequilibration
The preceding note on contingencies emphasizes the importance of environmental
change for the direction of emergent evolution. Environmental destabilization may
also reduce the agents of natural selection to a point where evolutionary experiments
have the freedom to diversify, prior to the inevitable re-establishment of ecostasis.
Disequilibration of homeorhesis makes epigenetic experimentation possible.
Destabilization of the internal milieu caused changes in primitive physiologies and
presented challenges that only improvements in adaptability could meet. To what
extent, then, is disequilibration important as a general evolutionary principle?
It is certainly of great interest to complexity theorists. In physicochemical systems
such as gases and fluids, temporary points of stability such as vortices, standing waves,
and local concentrations, are highly vulnerable to destabilization, though order may
be imposed by a phase shift such as crystallization that spreads through the system.
However, these shifts to more stable systems are reversible to more chaotic states. In
contrast, each emergent stage in progressive evolution collapses chaos as Cohen and
Stewart (1994) phrase it. In other words these are changes in order that resist further
interference. Greater degrees of physiological homeostasis also make the organism
more adaptable, more able to modify itself in ways appropriate to new environmental
conditions. This is not Lamarckian progressionism: many lineages have shown little
progressive change since they first emerged. I have also shown that advances in adapt-
ability can also regress into states that while less adaptable, conform better to the
limitations that ecostases impose on the availability of resources.
There may seem to be a paradox in the concept that homeorhetic and homeostatic
stability are products of emergent evolution. It is logically balanced by the realization
that they are accompanied by greater adaptability, and therefore freedom of choice.
And in some animal lineages that means freedom of behavioral choices that can
overcome tradition, both biological and social. At the latter level, a degree of chaos is
bound to return.
Closing Note on Baconian and Darwinian Epistemology
Francis Bacon had an intuition that the chaos of human society required Baconian
ordering in the form of a hierarchical division of laborunder the rule of philosopher
kings and their intellectually adventurous ministers. For him, there was only one way
to advance sciencehis way. Even his interpreters of nature were not permitted to
fly up to remote and most general axioms and then apply their supposed unshaken
truth to particular observations and experiments.27 Despite Darwins claim to espouse
Baconian principles, he took the other way, and his descendants have been doing it
ever since. If Bacon had always been followed dogmatically we would scarcely have
emerged from the seventeenth century. But doctrinaire adherence to Darwin has stuck
us in the nineteenth. Biology in general follows erratic paths between the two.
Consequently, sufficient particulars and minor axioms of evolution have accumulated
to allow us to ponder once more a synthesis that does not depend on the truism of
natural selection.
I trust that this makes the case that I am no more a Baconist than a dialectical
materialist. If the former, I would have stuck more strictly to Bacons rules of
tabulation, which require recording instances of the presence of a phenomenon;
instances of the absence of a phenomenon; and instances of change in the
phenomenon. Although all of these instances are in my brief, to stick to them too
formally would result in the long-windedness that he affected to despise. Similarly,
in the next chapter I am going to refer to a dialectical synthesis that does not conform
strictly to Hegelian or Marxist doctrine. For example, what I will call the thesis is
already a complex of complementary, not contradictory ideas. In the past they
remained dissociated because most intellectual nets were not cast widely enough, or
the few exceptions were treated with silence and contempt. Also, biology has become
a collection of splintered subdisciplines within which are plenty of pet concepts or
simply just metaphors that masquerade as explanations. However my thesis of comple-
mentary ideas must finally be united, if not in total harmony, with an antithetical
neo-Darwinism. A harmonious unification of opposites is a contradiction; for if
opposites can be unified they were only reified as opposites in pre-synthetic minds.
The punch line is that both Baconian induction and dialectical materialism are epis-
temological procedures that offer inductive guidance, and as such they deserve the
attention of students of biology. Any methodology can become a Procrustean bed that
requires the amputation or racking of thought until it fits.
10
An Emergence Theory
The state in which we now see all the animals is on the one hand the product of the increasing
composition of organization, which tends to form a regular gradation, and on the other hand that
of the influences of a multitude of very different circumstances that continually tend to destroy
the regularity in the gradation of the increasing composition of organization.
Jean-Baptiste Lamarck, 18091
[My concept of a] limited and contingent progress is very different from the deus ex machina of
nineteenth-century thought, and our optimism may well be tempered by reflection on the diffi-
culties to be overcome. None the less, the demonstration of the existence of a general trend
which can legitimately be called progress, and the definition of its limitations, will remain as a
fundamental contribution of evolutionary biology to human thought.
Julian Huxley, 19422
Transformation from the extremely unlikely to the likely is a major characteristic of systems
exhibiting emergent phenomena. Even when the simplest persistent patterns are infrequent in a
generating procedure, they will eventually occur if the system runs for any length of time. Once
they occur, they will by definition persist, making them candidates for combination with other,
persistent patterns (other copies or variants). At this point larger patterns with enhanced
persistence and competence can occur. . . . The usual argument that evolution requires long
sequences of improbable discoveries, and so is slow, misses this point. The unlikely will become
likely if one allows for a layered series of generating procedures.
John Holland, 19983
Evolutionary progress, as I have presented it, results from episodic emergences of

increasing, self-organizing, organismal complexity. Progress is induced and guided by
various intrinsic and extrinsic causes, among which particular actions of organisms are
important. Evolutionary emergences may be unpredictable saltations, or novelties that
appear at thresholds in continuous series of change. For Lamarck, however, progress
was gradual and continuous. Where gaps occurred, they were caused not by saltatory
emergences, but by environmental obstacles and adaptational distractions. Since
Lamarck lived in interesting intellectual and political timesin the milieu of the
364 Chapter 10
Enlightenment, the Industrial and French Revolutions, and not least the Fiber
Theoryone might have expected of him a more revolutionary concept of evolution-
ary progress. Perhaps evolution alone was revolution enough for Lamarck. In place of
divine law he called upon an inherent and steady progressive trend, the deus ex
machina to which Julian Huxley subsequently referred in Evolution: The Modern
Synthesis.
Like Lamarck, Huxley wished to explain how organisms had evolved from the
simple to the complex. He thought that natural selection, the ghost that Darwin had
put in the machine, as both cause and explanation of evolutionary progress, was
inadequate. Some of Darwins quarrelsome descendants have even greater difficulties
with evolutionary progress, and they often reject it as a delusion. But here we are,
discussing it! And there are our bacterial ancestors, who arent! Its not vainglorious to
say that we are different and more complex; to pretend otherwise is anti-intellectual.
An emergence theory must therefore accept the reality of progressive evolution, and
explain its mechanisms and processes. Huxleys approach was to amalgamate all the
pertinent aspects of biology, and he did a much better job of the Modern Synthesis
than the American version, which had a hard enough time simply pulling population
biology and genetics together with paleontology, and then losing the latter in short
order. Huxley also asked how some organisms could improve their general adaptabil-
ity, in contrast to organisms armoured against progresslocked into stasis by their
specializations. Huxley thought the adaptable, persistent types might advance further
if liberated into a more varied environment.4 He did not go so far as to say that they
were being liberated from natural selection. Nevertheless, his impatience with adapta-
tionism, and enthusiasm for progress as a product of developmental evolution led
finally to his exclusion from the hagiography of the Modern Synthesishe is barely
credited with giving it its name.
John Holland (quoted in the third epigraph) has the goal of finding the first
principles of emergence in simple systems that can be mathematically formulated. He
is concerned with persistent patterns that complexify by new combinations of variant
building blocks as the system increases in size. Therefore his thesis emphasizes
autonomous emergence by repetitive differentiation. Yet it does not exclude extrinsic
causes that might effect epigenetic events and genetic mutations. All of this is relevant
to progressive evolution. And although Holland does not refer to progress per se, it can
be inferred from his remarks about complexity increasing through reorganization. It is
also implicit in his statement that requiring evolution to be a long, slow sequence of
improbable discoveries misses that point.
At this juncture, I share Julian Huxleys goal of clarifying progressive evolution,
while I reject natural selection as its cause. In this chapter we will reach for a theory of
emergent evolution by integrating the subtheories surveyed in the previous chapter. A
dialectical synthesis that would accommodate both emergent evolution and the
An Emergence Theory 365
hypostasis of dynamic stability is desirable, and possiblebut only at the higher epis-
temological level of the history of life. That will be attempted in the final chapter. In
the meantime, we must not reject the selection syndrome outright. For one thing the
consequences of progressive emergent evolution penetrate the early stages of re-equi-
libration as adaptational evolution leading to specialization and ecostasis. Moreover,
we must take the selection syndrome into account as a prevalent constraint in the
history of life, and consider how dynamic stability provides a pause during which
sudden innovations can shake down into smoothly interacting modules and wholes.
Then we can further explore how its obstructiveness has been periodically overcome.
We have attended performances in the causal rings of the evolutionary circus,
exploring association, physiology, behavior and development, and we have seen how
they leap and swing and interweave in patterns under the big top of the environment.
Emergent evolution has been sorted into categories of intrinsic and extrinsic causation
as well as saltatory and critical-point processes. And I have summarized their
mechanisms, along with the contingencies that affected their course and enhanced
their operation. Now for a recap of universal features, before a deeper plunge into the
dim depths of formal theory. Important points that have been discussed earlier are
interpolated in brackets, to remind us that there are subalterns under the generals.
Then the theories of symbiosis/association, physiology/behavior, development and
environment can be integrated into a more natural system.
Evolutionary emergentism implies discontinuity in the generation of novelty. Even
a mutation that gives rise to a minor phenotypic variation is discontinuous.
Emergences may occur at critical points in a continuously evolving allometric series,
suddenly bringing functional novelties into play (gliding to flight). Saltations may
emerge from a spontaneous coming together of appropriate generative conditions
(origin of life; endosymbiosis; sex; multicellularity). Or they may be due to repetitions
and rearrangements of existing conditions (codon, exon and gene duplications and
differentiations; exon and protein domain shuffling; gene transposition and
conversion; chromosome mutations; homeotic shifts). Divergent saltations may leap
in new directions from generative thresholds, at intermediate stages in established
continuities of embryonic development (radical deviations, larval digressions that
return to the adult norm, innovations arising from paedomorphosis). Emergences may
be largely intrinsic (self-generating, or autonomous) or extrinsic (imposed by or
responding to the environment), but hardly ever exclusively one or the other. Their
persistence is often characterized by adaptability, multifunctionality, and ontogenic
flexibility.5 And these amount to an integrated noveltya whole that is greater than
the sum of its parts (quaternary protein structures, contingent interactions of
molecules or physiological systems, symbioses and societies).
Emergences are generated by natural experiments involving mechanisms of
repetitive differentiation, mixing and matching, heterochrony, exploratory behavior
366 Chapter 10
(both developmental and organismal), physiological and behavioral responsiveness to

the environment, and unpredictable external contingencies (physicochemical,
climatic, catastrophic impacts). When molecular biologists talk about episodic
evolution there is usually duplication of a gene or a genome at the heart of it (growth-
hormone genes, genome duplication and reduplication in early vertebrates). These are
crucial evolutionary processes, but the emergence principle applies at all the higher
levels, from organogenesis through organismal physiology and behavior to the inter-
actions of societies and communities.
Emergences are episodic, lacking periodicity and hence predictability. But are they
altogether random? Darwin assumed total randomness in most biological change,
because omnipresent, non-random, natural selection would ensure that adaptive
random changes were saved and reproduced. (Moreover, selection theory would also
be saved and reproduced!) Emergentists, unlike Darwin, are not trying to impose
randomness of evolutionary change in order the magnify the importance of natural
selection. We are more directly concerned with the causes of evolutionary change, and
therefore able to recognize that many molecular changes are non-random (hyper-
mutability, transposable elements, self-amplification), and with how the extremely
unlikely becomes the likely. Moreover, the significance of random change depends on
where and when it happens. If it occurs in the context of appropriate generative
conditions it may catalyze an emergence with a constellation of novel qualitiesa
whole that is greater than the sum of its parts. For example, a purine synthesized in
an interstellar dust cloud might persist, yet would be unlikely to participate in a
biological emergence. In contrast, a purine synthesized in a wet place containing other
abiogenic organic molecules is a lot more likely to be involved in some kind of
emergent system. I will discuss this further in the context of Hollands layered series
of generating procedures.
Once biological emergences appear, they fall into dynamically stable organismal
and ecological states that resist change. Paradoxically, the higher the level of
emergence, the easier it becomes to escape stasis. This is because of greater freedom of
choice for the organism, and more alternatives of habit and habitat from which to
choose. My zoological bias is again disclosed by this statement, but the same applies
to plants to a less obvious degree. Though neglected by reductionist evolutionists, the
bootstrapping interaction of development, association, physiology, behavior and
environment has been to the fore in animal evolution. As a result of such feedback,
internal stasis can be disequilibrated from without. Also, ecostasis can be disrupted by
large-scale emergences, avoided if the emergents move to unexploited environments,
or simply eradicated by catastrophe.
Saltations can leap the barriers of stasis. The clearest examples of truly saltatory
emergence are to be found in the associative arena, with epigenetic deviations
following close behind. Coalescence of self-reproducing proto-bionts generated the
first self-repairing and self-organizing cells. Endosymbiosis and sexual association,

which were the next major emergences, brought an array of physiological and
behavioral changes with them, even at the unicellular stage. Principles of association
and epigenetics apply to the differentiation of multicellularity, another foundation of
emergent evolution. The disadvantages of independence are turned to the advantage
of the whole. Thus, improved wholeness, because it is more artful at getting out from
under the agents of dynamic stability, is a formal characteristic of saltatory emergence.
Although, for the moment, epigenetic innovations are subsumed as part of the
potential provided by multicellular associations, emergences of the distinct body plans
of the animal phyla deserve particular emphasis, and these also illustrate saltatory and
critical-point processes.
Associative emergences have had the most significant biotic impact on geophysiol-
ogy, initially through the oxygenation of the biosphere. Once they invaded the land,
symbiotic fungal-algal plants constructed soil, extended their range, and affected
global albedo and climatic patterns. For emergent plants and animals, novel physico-
chemical conditions had immediate direct impact on functional morphology.
Symbiosis continued to have major consequences. Photosynthesizing symbiosis, in
conjunction with rigid plant cell walls, effected progressive ecosystematic changes and
raised oxygen levels in the air. Cellulose became the foundation of a new trophic
pyramid once animals acquired symbiotic micro-organisms to digest it. Plant
evolution extended diversity of habitat for animals, and correlated changes in animal
habits affected their morphology. However, the greater their physiological and
behavioral adaptability, the more they could take advantage of the full range of
available environments.
The last great emergences, intelligence and mind, were products of developmental,
physiological, behavioral, and social evolution. Some elements may have simply
appeared at critical points in the expansion of the cerebrum, the increased capacity of
its neurons to form new dendritic connections, and repetitive variation of chemical
messengers that allowed the brain to distinguish between new functions.
Nevertheless, epigenetic algorithms, orthogenesis and constraints, directional
selection, and hypermorphosis are insufficient explanations. For example, the allo-
metrically expanding hemispheres of the cerebrum benefited from a new link, the
corpus callosum. That integration then bootstrapped further hypermorphosis, since
the two hemispheres could become more differentiated without being of different
minds. Innovative integrations of brain areas for logic, language, memory, vocaliza-
tion, and aesthetic sensibility were part of the emergent constellation. To be
meaningful they had to be connected with hand-eye coordination. To be fully
effective they had to be able to override older, hereditary, behavioral mechanisms.
This required further reorganization and bypassing of existent neural connections.
The emergent result was greater freedom from gene determination.
368 Chapter 10
The evolution of this web of dynamic structures occurred in a broader environmen-

tal context. Big-headed babies could develop fully and survive only if their mothers
were well nourished, so they needed extended families. Putting it another way,
extended families were part of the generative conditions that allowed big-headed
babies to become successful monsters. Once they survived, they needed social
interaction to continue their neural complexification to the point where its adaptabil-
ity could be fully exploited. Unfortunately, one of the larger consequences of
socialization is a renewed assault on geophysiology, through deforestation, greater
carbon dioxide production with its greenhouse consequences, and emissions that
destroy the ozone layer. Geophysiology will always be in some kind of homeostasis,
but not necessarily one that is kind to interfering humans.
An Emergence Theory holds that evolution is emergent, and explains its generation,
and its qualities. It might emphasize intrinsic or extrinsic causes, but does not stray
too far from a holistic, or interactionistic evaluation of evolution. Nor does it simplis-
tically characterize evolution as either saltatory or gradual. In resolving these apparent
contradictions an emergence theory shows dialectical competence. The generative
conditions of emergences combine interacting associative, physiological, behavioral
and developmental causes. Post-Lamarckism (with its emphasis on the causal nature
of external factors, but without the inheritance of acquired characters) is integrated.
The syndrome of secondary causes and effects known loosely as natural selection is
interpreted as barely adequate to simple adaptational evolution, but more importantly
as an ultimate obstacle to the evolutionary diversification of subsequent emergents.
Phenotype sorting, differential survival and reproduction, and agents such as
competition, predation, and sexual selection are recognized as the consequences of
emergent evolution. Nevertheless, phases of intrinsic and extrinsic dynamic stability
provide time for the shakedown of emergent novelty.
Selection theory is not only secondary to evolutionary causation, it also lacks
historical priority. That falls to Lamarck, who for all his inadequacies and errors saw
progressive evolution as the thing to explain. And priority over neo-Darwinism falls to
the neo- (or post-) Lamarckists, who not only addressed the right issues, namely
generative causes, but gave them a far more holistic environmental context.
Does Emergentism Provide an Adequate Theory of Evolution?
That evolution is a historical reality was proposed by Lamarck and established by

Darwin. Whatever doubts remain about the chronological details and phyletic
affinities, the historical theory has become axiomaticnot just a theory (which
many non-scientists or non-philosophers equate with just a speculation). It is the
theory of causation, or the evolutionary mechanism, that is at stake. Emergentism
might be colloquially referred to as a theory, but to really qualify it would not only
need to increase the understanding of the relevant phenomena. It would also be

expected to make an inspiringly simple, formal statement about its nature; preferably
mathematical or at least translatable into something quantifiable. It should give some
indication of where to look for mechanisms and how to experimentally test them.
A formal theory of emergent complexification would have to address not only
generative causes, but distinguish between the two different processes of saltatory and
critical-point emergence. Then there is the category of haphazard contingency, which
includes a multitude of feedbacks from environment to organism and back again, and
includes the evolutionary significance of catastrophe.
I have been ignoring the applicability of emergentism to non-biological
phenomena, partly because of my bias as a biologist and partly to keep matters simple.
Most current theoretical studies of emergence do not involve biological systems but
presume to infer biological significance. The emergence of biological reproduction was
a major discontinuity. It also, with the corollary qualities of self-maintenance and self-
organization, established the novelty of biological evolution. Therefore, I have always
balked at making the emergences of life an extension of cosmological evolution, in the
original sense of unfolding or unrolling. I suspected that a try for an Emergence
Theory of Everything could effectively produce an Emergence Theory of Nothing,
especially if physical principles are expected to be its generators. A catchy name that
purports to save all the appearances does not make a theory, whether it be
emergentism, synergism, natural selectionism, or Lamarckism qua the
inheritance of acquired characteristics. Yet, during the time I have spent on this book
I have come to the opinion that a complete synthesis should accommodate all natural
phenomena, from the cosmological to the cognitive.
Several complexity theorists who understand the importance of emergence have
tried for mathematical abstractions that would apply from physical phenomena to
biological evolution. It cant be done, because new rules appear with every new
emergence. In Signs of Life (2000), Ricard Sol and Brian Goodwin effectively
demonstrate how mathematical descriptors of emergent systems can be achieved. But
a mathematical descriptor no more explains how an emergence originated than
a landscape painting explains how the landscape came to be. Both may provide clues
to the unknown, and both have large audiences that are comfortable with the
techniques, and enthusiastic about the resultsconsequently more minds are ready
to invest in the subject. However, there is one proven mathematical approach to
the generation of change, with which many modern biologists are familiar: the trans-
formational theory of DArcy Thompson. The coordination grid diagrams from the last
chapter of his book On Growth and Form (1917) are still frequently reproduced
to demonstrate that change of overall form, in skull structure, for example, fit mathe-
matical formulae. Therefore their generation is either driven in part, or at least severely
constrained by mechanical forces. That seems to indicate how a mathematico-
370 Chapter 10
reductive approach can successfully be taken to critical-point emergence. DArcy

Thompson was himself wary of oversimplificationhe admitted his omission of the
essential biological mechanisms that actually did the building in obedience to the
mechanical constraints and forces.
The more you try to dissect emergent evolution the more it holds togetherno the-
oretically dominant reduction, mathematical or otherwise, pops out. Furthermore, for
a comprehensive theory, due attention needs to be paid, not only to all the parts, but
also to the exceptions and contradictions. Those are what mathematical formulations
are likely to miss. The best theory must model a web of related causes and effects and
must show how emergent features originate, how they affect all the other causal
strands, and how they all connect to the biospheric whole. Emergentism does not
have to qualify technically as a theory to demand that more attention be given to the
generation of novelties, and less to their subsequent demographic fate. That would
certainly clarify evolutionif shifting to the relevant from the irrelevant matters.
Theoretical Potential
A simple way of testing the theoretical potential of emergentism is to ask how it would
change traditional interpretations of evolutionary history. The conviction that
evolution is a real process that followed a particular historical course was instilled by
evidence originally set out in The Origin of Species. Much of that evidence has proved
incontrovertible. Early molecular biological evidence that partly explained the origin
of variations was added to what had already been concluded from functional
morphology and embryology, but awkward questions about gene expression were
ignored. Now, if the completion of the human genome project has demonstrated
anything of value to evolutionary theory, it is that knowing the genes is not nearly
enough. Some of us were already aware of that before the project was undertaken.
We do not need a new theory to tell us that that evolutionary history was discon-
tinuous. The evidence has been staring us in the face ever since marine fossils were
discovered by the ancient Greeks in strata high above sea level. Later, demarcations
between the strata could be seen to have been imposed by sudden catastrophes or
rapid climatic changes, as Cuvier said nearly 200 years ago. We can also surmise that
discontinuity was generated by autonomous evolutionary emergence as well. One of
the consequences, in vertebrate evolution at least, was a growing potential for
behavioral adaptability that had a positive feedback effect on further emergent events.
All genetic molecular changes are saltatory, many are non-random, and some are self-
amplifying. The molecular biology of embryology and homology also supports
saltatory epigenetic interpretations. And the more discontinuity of evolutionary
history is illuminated, the dimmer becomes the light of Darwinian gradualism.
The fossil record, and the diversification and numerical distribution of modern
organisms, suggest which emergences have actually been most significantmost
analysts settle for life, sex, the eukaryotic condition, epigenetic complexification, and
mind. Progress to new emergent levels, and the components of advances in adaptabil-
ity, can be tentatively identified. Artificial selection, a bulwark of the Darwinian
historical theory, is a better model for the performance of emergent novelty in the
absence of natural selection than it is for the creativity of natural selection. Thus, some
of Darwins original evidence can be removed, some reinterpreted, and some reversed.
The superstructure of the Modern Synthesis could be renovated out of nostalgia, but a
new theory is needed to integrate new historical and causal interpretations of
emergent evolution without the stultification of selectionism.
How much can we get out of an emergence theory at its present inchoate stage of
construction? It proposes that the first living cell, with the emergent properties of self-
maintenance and reproduction, contained the potential for progressive evolution.
Emergent novelty could suddenly appear at critical points or thresholds in allometric
evolutionary continuities, or through qualitative saltations. Preservation of integrity
at every stage is a given, but that quality alone gives no guarantee of survival or success
in the face of strong competition and predation. Therefore emergent evolution was
unlikely to succeed unless its products had immediately advantageous properties that
made the old competition irrelevant. (Recall that such properties are inherent in the
emergence, not created by prevailing extrinsic circumstancesthough perhaps, by
chance, appropriate to them). Alternatively, emergent properties allowed the
discovery of environments where agents of natural selection were absent, or had been
removed. Hence the congregation of adaptable organisms at environmental interfaces
was important for evolutionary progress. These circumstances were pivotal, but so rare
that successful progressive changes were brief evolutionary squirts, interspersed with
periods of diversification, and longer periods of dynamic stasis.
When major emergences occur they bring with them new rules of operation that
can only be predicted in very general ways from a knowledge of lower levels of
emergence. That simple life could become more complex is predictable enough.
However, to abstract principles of complexification to a new emergent level, theory
requires the canny approach taken in Hollands Emergence: Order from Chaos (1998)
and by Sol and Goodwin in Signs of Life (2000). Following that route it might
ultimately be possible to write an epigenetic program for the developmental complex-
ification of a specific type of zygote. Remember, however, that a complete description
of the process in an animal with a completely charted genome, such as the nematode
worm Caenorhabditis elegans, does not explain it. It takes us part of the way, since it
might suggest how new algorithms might have emerged from the epigenetic nodes.
Yet such abstractions are complicated by environmental, associative, physiological,
and biochemical variables. The algorithms in question operate through different
factors at every hierarchical levelenvironmental or organismalas well as through
the genes and their protein products; however, the algorithms are not determined by
372 Chapter 10
genes. Components that do reside in genes have been historically instructed by the
organism and its environment. Whatever information the genes might consequently
have, they need to be told what to do by higher organismal levels.
The basic instruction embedded in an algorithm is If this is the current situation,
then that is the necessary response. And for an organism to do that, it needs more
than the genes; it needs modifiers, signals, functional morphologies, and experiences
that constitute this. Furthermore, the constructive impact of this is accompanied
by negative effects. For example, progressive DNA repression, methylation and histone
binding constrain how much of that might be possiblea necessary means of
separating organismal offices prior to the refinement of their concurrent efforts. This
ensures that the ontogenic whole is not only greater than the sum of its parts, but quite
different from the whole that constitutes the early embryo. The course of cell-line
differentiation and the dynamic form of the mature organism are results of non-linear
processes. Their evolutionary pathways cannot be predicted from a simple generalizing
principle. Even if they could, the routes of their progress are influenced by contingen-
cies that are themselves partly to be expected and partly a matter of pure chance. Thus,
the parsimony of Its all in the genes is as spurious as that of God did it.
Sidney Brenner, who originated the C. elegans studies, has come to understand that
the genetic information is not enough, and that theoretical biology must deal with the
flow of that information.6 To do so requires a holistic/interactionistic ability to
integrate all of the factors operating at every hierarchical leveland a practical as well
as theoretical facility with biology.
Apart from the materialists truism that life has no programmer, there are interesting
parallels between progressive improvement of the design of mechanical artifacts, and
the evolution of organisms. Electronics, for example, followed a progressive sequence
of experiments punctuated with key discoveries like an alternating current electricity
supply, servomechanisms, diodes, transistors, and microchips. Between inventions,
societies explored their uses and exploited their benefits, although some novelties that
defied application were shelved for the time being, and then dusted off when their
potentials were recognized. These engineered emergences provided both economic
and theoretical boosts, and their uses often diversified widely. The electronically
engineered future is somewhat predictablehigh-temperature superconductors,
biochips, and fuzzy-logic computation are being pursued. To stay with the engineering
parallels, biological evolution progressed to becoming greater wholes by acquiring
add-on parts, through symbiosis, and through multicellularity. Once there, surplus
capacity made redundant components available for retooling at the molecular and
organismal levels. Although the analogy takes us part of the way it is insufficient to
clarify biological evolution. There is still a ghost in the organismal machine.
For an organismal whole to become greater than the sum of its parts it must be pro-
gressively self-engineering. A creature with a multiplicity of parts needs a hierarchy of
regulators to become an organized complexfirst, promoters of protein synthesis that

respond algorithmically by binding peptides and steroids; next some kind of
hormonal system that produces those activating and inhibiting molecules, and so
directs epigenesis, and signals between cells in the mature organism. Then (in the case
of animals), a central nervous system to provide rapid and dedicated communication.
These kinds of complexifications yielded greater functional efficacy and energetic
efficiency. There were key innovations along the way, such as the myelin that
insulated the wiring and speeded up signals without being anatomically unwieldy, and
the emergence of migratory neural crest cells that complemented these and other
functions. And then there came rerouting and retrofitting to bypass primitive
command centers without interfering with their essential functions. The emergence of
the corpus callosum connected the increasingly isolated cerebral hemispheres. But the
basic physical and biological mechanisms for generating electrical impulses were
already present. Neurons are omnipresent in the simplest and most primitive multi-
cellular animals. Nervous systems co-evolved with hormonal systems that worked by
diffusion before the emergence of body-fluid circulation. Such systems are always
subject to phenotypic modification by the actions of the organism and the
environment, as well as genotypic modification. If the parallel is made with an
automobile, not only must it be re-engineered while still in motion with all systems
go; in addition, its modification is directed in part by the route it is taking. There is
a pit stopsexual reproductionduring which the whole vehicle is rebuilt. But
although the genetic engine is re-organized and repaired at that stage, it is also
maintained and modified by maternal mechanics. They not only provide fuel and
spare parts for the early part of the next lap, their quantity and redistribution can
cause drastic changes in the phenotypic track performance of the vehicle.
The Predictability of Emergences, and the Predictiveness of an Emergence Theory

Conventionally, scientific epistemology requires that any formal theory should
predict the consequences of a given set of interacting conditionsin particular, the
likely results of scientific experiments. Such predictiveness should focus ideas, research
and experimental design, whether through practical or thought experiments.
Paradoxically, emergences are generally believed to be unpredictable, the reverse of the
coin being that wholes that are greater than the sums of their parts are irreducible.
One of the stumbling blocks to comprehension is that redundancy and circularity
tend to creep into definitions of predictability. For example, it is not helpful to be told
that non-linear dynamics are characterized by unpredictable resultsthen to be told
that because emergent effects are unpredictable they must be the products of non-
linear dynamicsthus unpredictability is a sine qua non of emergence. There do exist
emergent wholes that can be entirely reduced, but such an exercise does not remove
the whole nor its emergent properties from further consideration. In any case, the
374 Chapter 10
putative unpredictability of emergences, and the predictiveness of an emergence

theory are two epistemologically distinct issues. It is quite consistent for a theory that
deals with unpredictable phenomena to be predictive in the sense that it can guide
empirical and theoretical research. Predictability of events, and predictiveness of
theory have a tenuous logical connection. Therefore, I deal with both in this section.
C. L. Morgan surmised that we could not predict emergences because of our
imperfect knowledge of their antecedents. Thus, if we dug deeper and thought harder,
predictability might be achieved. However, in the natural biological world, the
generative conditions for emergences contain too many variables. And there are other
problems. All known biological emergences are historicalwe can only make
reductive sense of them through hindsight. Second, the nature of future emergences
is in the realm of science fiction. There has been no shortage of predictions of that
kind, and time and again those of a linear technical nature have come to passspace
ships, artificial satellites, moon landings, space stations, and so forth.
The unpredictability of emergent properties is an aspect of their novelty relative to
the older, simpler levels of the hierarchy. Physical phenomena such as superconduc-
tivity, superfluidity, ferromagnetism, and crystal structure have emergent properties
that would not have been predicted from physical principles and elemental
chemistry.7 By John Stuart Mills example, a complete knowledge of the properties of
oxygen and hydrogen would predict the empirical formula H2O, and might suggest
some qualities of its gaseous and crystalline phases, but would not predict the every
snowflake is different aspect of ice formation. A knowledge of the behavior of waters
hydrogen bonds would predict anomalous properties of its liquid state. But it helps a
lot if an a priori knowledge of the emergentwateris smuggled down to its
generative level. Ricard Sol and Brian Goodwin (2000) carry the discussion beyond
this point by demonstrating that the Navier-Stokes equations that circumscribe the
behavior of water are based on its properties of incompressibility, cohesion, and
fluidity, none of which are predictable from a knowledge of hydrogen, oxygen, or the
water molecule in isolation.8 In turn, the Navier-Stokes equations are incompetent to
predict Bnard cellscomplex, orderly patterns of fluid flow that arise from changes
in thermal gradients. These too can be captured mathematically once they have
emerged and have been quantified. However, reducible complexes are not necessarily
predictable from physicochemical principles.
Some biological emergences are completely reducible. The tetrameric mammalian
hemoglobin molecule has the emergent property of cooperativity, which makes
oxygen loading and unloading much more efficient than is possible for the four
constituent monomers acting alone All of that can be explained reductively, provided
the necessity of having an organism to synthesize the molecules is left out. However,
there are radical differences between physicochemical and biological emergences. For
example, before they ever met in appropriate circumstances, atoms of oxygen and
hydrogen already had the propensity to combine as a peculiar liquid at the appropriate
temperature and pressure, with all of the properties allowed by the hydrogen bond.
Simple molecules of H2O can become more complex structures, such as Bnard cells,
icebergs, waves, and whirlpools. But those are temporary states of complexity that are
easily undone back to a simple compound or its elemental components. Therefore,
although the complexities of water are unpredictable, once they are known they are
reducible to physical properties. Therefore, water is distinct from evolutionary
emergents that depend not only on changes in the simple constituents but also on
biological reproduction, a hierarchical foundation of earlier emergences, and multiple
contingencies. Copy error is a major component of emergent evolution that does not
apply to non-living systemsunless there is a deus ex machina, in the form of a human
experimenter who makes it so. Moreover, if there are any Special Creationists or
Intelligent Designers still with us, what, pray, would be the point of a capacity for
making mistakes, as opposed to the creation or design of exactly what was wanted?
All known evolutionary emergences have already occurred, and Sol and Goodwin
have done a creditable job of showing that their qualities can be discovered, captured
by mathematical descriptors, and demonstrated not to contradict rules operating at
their generative level. The question of predictability of higher levels from the qualities
of lower levels needs to be tackled with honest post-predictions that ask whether
knowledge of the generative level could have allowed prediction of the new focal
levelno smuggling down of its emergent properties allowed! The pragmatic problem
for biologists is: how were known emergences generated?
Some critical-point emergences seem to be linear and predictable. I refer to self-
amplifying allometric shifts, such as the increase in the size of a forelimb that lets it
function as a wing with true flight, at the point where lift exceeds drag. It is true that
the aerodynamics of flight was not captured mathematically until it had been
observed as a real function, but all kinds of predictions could be applied from simple
models to untried biological aviation experiments. Here the unpredictability problem
would seem to be spurious, but it has to be compounded with the metabolic and
behavioral and environmental requirements. Whatever the answer, I am not going to
exclude these kinds of innovative critical-point biological emergences just because
they cant be stuffed into the pigeonhole of unpredictability. Some philosophers save
them by calling them weak emergences, in contrast with strong saltatory
emergences. The problem of predictability is compounded by contingencies that sig-
nificantly affected the course of evolution. However, symbiogeneses, earthquakes,
volcanic eruptions, and bolide strikes are probable, if not predictable as to timing.
Holland suggests that a long-running experiment in the combination of persistent
patterns will inevitably result in their complexification at higher emergent levels. That
the unlikely becomes the likely under these circumstance is a predictive generaliza-
tion, but Holland adds that such effects are unpredictable. As a human organism he
376 Chapter 10
intuitively knew that before he became a theorist. It may be predicted that emergences
will keep on happening; its the timing and the exact nature of a particular emergence
that is unpredictable. Furthermore, their occurrence can be narrowed down from
global to local generative sites. A likely location for natural experimental freedom is
where one ecosystem meets another, where their constituent organisms can interact.
Others are interfaces between physicochemical or biological systemswhere clay and
detrital surfaces meet the water columnwhere the organismal epidermis meets the
external milieuwhere the non-adaptable is torture-tested. At the microscopic level,
typical venues are where cells or molecules come into contact at cell membranes,
especially synapses, junctions, and intracellular membranes and microtubules. At an
even lower level, the surfaces of proteins, the way they fold, and their interactions
with water molecules, ions, organic compounds, and each other, have emergent
potential.
David Rollo (1994) argues that the problem of predicting the emergent stems from
the astronomical combinatorial possibilities for multiple holonic variants at the
generative level. But the same difficulty would apply to the epistemological process of
inducing any effective hypothesis from among an infinity of options. The problem is
routinely overcome by lateral thinking, or intuitive inference, and alertness to the
unexpected.9 One commentator on emergence tells me that predictability is a red
herring, meaning that predictability and non-predictability are unnatural categories
imposed by the limitations of logic. If that is so, we should simply ask the obvious
questionsCan emergence occur, has it occurred, and will it occur?and we should
anticipate the obvious answer: Yes. The hypothetical possibilities for biological
emergence are limited by boundaries of integrity, beyond which disintegration is their
likely fate. Yet the following general predictions can easily be made:
Predictable Changes
1. Self-maintaining integrity and the ability to reproduce and differentiate are
emergent properties of the first living systems. With those qualities they will
inevitably become more complex, especially if they are made up of reproducible
modules, such as DNA, cells, and organs. This is a post-prediction as far as living
systems are concerned, but is predictable from non-biological complexity models.
2. Out of an array of redundant genes, some of their variants will serve novel
enzymatic, hormonal and other regulatory functions that increase complexity.
3. There are corollaries to 1 and 2, at and above the gene level: in a holonic (or
modular) system that is organized into a hierarchy, change in redundant holons can
increase the complexity of order. Some of the older systems may be bypassed or
reorganized.
4. Simple organismsproto-bionts, prokaryotes, eukaryoteswill form symbiotic rela-

tionships with each other and with more complex multicellular organisms.
5. Unicells will form multicellular complexes, which will ultimately differentiate.
6. Complexity will also be generated by topographic changes that affect the expression
of homeotic gene clusters and by movements of embryonic cells that effect develop-
mental organizational changes.
7. Hierarchical layering is both spatial and temporal in organisms. During

development the branching and interaction of cell lineages follow algorithms that are
susceptible to heterochronous variation. In the mature organism the spatial layers
(molecules, cells, organs, whole organism) interact constantly. They will be further
influenced by temporal changes that are either random or cyclical.
8. In practical terms hierarchically ordered complexity may be governed by physiolog-

ical communication such as hormonal and nervous systems, i.e., both wireless
broadcast and hard-wired. These are subject to emergent changes.
9. Differentiation at the organismal level can lead to phyletic divergence. It is

predictable that diverse types may become concentrated together in the same place at
the same time. Therefore it is predictable that symbioses and looser associations will
emerge in such environments.
10. Symbioses and other emergences can also reshape the environment to make more
diverse ecosystems that are initially free of agents of natural selection such as
competition and predation.
11. Environmental interfaces will be inhabited by adaptable organisms, some of which

will penetrate to the adjacent zone, exposing them to physiogenic change.
12. External, internal and intracellular environments will impose physicochemical

change. Organisms will respond behaviorally, physiologically, and at the molecular
level.
13. Terrestrial plants will experiment with the a variety of forms that will establish
major ecosystems. (Tree forms produce forests, grasses produce savannas, and so on.)
14. In some animals, experiments in behavior will tend at first to be genetically

assimilated. Then they will tend to escape to greater degrees of individual freedom.
378 Chapter 10
Progress in behavioral evolution, if unconstrained, will increasingly influence the

nature of functional-morphological emergences. (E.g., insect size is physically
constrained by the exoskeleton, which limits the size of the nervous system, which
restricts them to stereotyped behavior patterns.)
15. Environments with stable high temperatures will physiogenically impose a quasi-
homeothermy on their inhabitants.
16. Thermogenesis, insulation, and the construction of microenvironments will allow

some animals to behaviorally experiment with cooler environments.
17. With dependable homeothermy will come the expansion and complexification of
the central nervous system, producing more exploratory or curious behavior until
intelligence emerges.
18. Social interactions will produce effective wholes beyond the organismal entity.
It would be simple enough to select an appropriate progressive series of emergences,

and conclude that it has to be that way. Julian Huxley remarked:
Evolution is thus seen as a series of blind alleys. Some are extremely shortthose leading to new
genera and species that either remain stable or become extinct. Others are longerthe lines of
adaptive radiation within a group such as a class or sub-class, which run for tens of millions of
years before coming up against their terminal blank wall. Others are still longerthe lines that
have in the past led to the development of the major phyla. . . . But all in the long run have
terminated blindly. . . . Only along one single line is progress and its future possibility being
continuedthe line of man.10
The octopus, for example, achieved some kind of intelligence without going through
all of the stages required of homeotherms. Once there, it could not take advantage of
its flexible behavior to progress further. It was in a blind alley because its general phys-
iological adaptability was inadequate for further change to a freshwater or terrestrial
existence. Yet this shows that a variety of routes to the emergence of complex
organisms might be taken, and that despite the advancement of humans we are not
the only model worth investigating. There are some inductive guides to focus
prediction of progress. Evidence of an allometric or proportional growth shift in the
past predicts the possibility of its exaggeration in the future, and novel functions may
emerge at critical points. Allometry and molecular homology also give parallel and
convergent shifts some predictability. Natural selection will be manifested in consoli-
dation of the gains of emergent experiments. The consequent dynamic stability will
present barriers that only saltatory experiments will leap over, and that only
autonomous drives will be able to ignore. Predictability of emergence as it has just
been outlined is qualitatively different from empirical predictiveness. So now we have

to ask if emergentism has enough predictiveness to suggest experiments to refute its
own implications, as distinct from assessing the post-predictability of particular
emergences that have already occurred. Can it point to obvious avenues of research to
which the older theories did not point? Has it a unifying formal structure that applies
to a broad spectrum of biological phenomena?
Emergentism predicts that conditions where the barriers of natural selection are low
or absent will encourage the numerical increase of existing emergent types. Natural
experiments may often have failed because such opportunities were too rare.
Nevertheless, the more adaptable an organism becomes, the more operational freedom
it has, and the greater scope to diversify. This is a dimension that enlarges the
unoccupied niche space of neo-Darwinists, and the morphospace of developmen-
tal evolutionists. However, as diversifying emergents multiply in ecospace, dynamic
stability will be re-asserted; new wholes will become more finely tuned, and future
emergences will have more hurdles to leap. Therefore, progressive evolution, whether
structural or functional, must, on the rare occasions when it happens, advance by
saltation: not just genetic, sometimes behavioral, and sometimes amidst cataclysmic
clearing of laboratory benches. Problems of predictability and predictiveness can be
addressed by thought experiments, and may not be beyond observations and
experiments in the field or in the laboratory, but for there to be a way there has to be a
will. In the meantime, scientific analysis has largely employed computer models that
are unavoidably simplistic.
Empirical Tests
Whereas selectionism addresses the maintenance of the status quo, emergentism is in
a position to institute new interpretations of evidence already available. The historical
records of artificial breeding programs, for example, provide a wide range of data
pertaining to the fate of phenomena that appear and persist under what Darwin
referred to as the changed conditions of life. Dmitry Belyaev (1970) called it destabi-
lizing selectiona misnomer, since differential reproduction did not come into the
case, and he meant that it was an array of effects caused by a variety of living
conditions. The agents of natural dynamic stabilization were absent through human
manipulation, but hormonal/behavioral bias, genetic isolation and founder effect
were imposed. With some attention to emergentism it should be possible to
manipulate variables in breeding experiments more appropriately. And the effects of
eliminating the differentiality of survival and reproduction are testable. Emergentism
would also encourage greater investigation of naturally destabilizing conditions,
whose potential was suspected by Belyaev and his predecessor Ivan Schmalhausen.
The original question that brought us to this pass was Does emergentism give rise
to a new causal theory of evolution?z Its causes, effects, and categories of emergence
380 Chapter 10
differ from those proffered by the Modern Synthesis not only in re-inventing natural
selection and emergence. It also has some power to direct future analysis and
synthesis, and to predict future events as well as post-predicting the generalities of past
evolution. It is non-Laplaceanaxiomatically unable to tell the future history of life
in any detail from a total knowledge of life as it is. But it does say that life will progress,
and that the end of natural selection is not the end of evolution. The reverse is true.
We already have the means to modify our future evolution, without anything like
natural selection having a role. We can make specific changes and proceed from there.
Going back one step in history, plant and animal breeders worked with natural
experiments that might have arisen coincidentally from conditions that they have
imposed. Again, natural selection was excluded. Nature does much the same with its
experiments. Its successes arise from their qualities. Natural selection is no more
relevant there than it is with deliberately designed modifications.
Karl Popper alarmed theorists when he inferred that it was impossible to test a null
hypothesis for natural selection, as defined by neo-Darwinists, and that selection
theory was therefore unscientific.11 But null-hypothesis experiments on natural
selection have been going on for about 10,000 years, without the experimenters being
aware of it. Plant and animal breeders have always done their best to remove the
influence of natural selection, so that any sports or hopeful monsters that seemed
interesting or useful to them would be preserved from competition, predation, disease,
the vagaries of climate, and genetic dilution. Embryologists and epigeneticists ensure
that such agents of natural selection are minimized. If they were to recognize this, and
act upon it, they might better understand how natural experiments occur and succeed,
and also grasp the role of natural selection in consolidating saltatory emergences. J. W.
Beaments observations on how competition limits the full expression of the potential
of an animals adaptability could be an inductive guide for such investigations.12 And
the heuristic computer models developed by complexity theorists are improved by
factoring in progressive adaptability as well as a re-invented natural selection.
Beyond predictions about the course of evolution, a well-knit emergence theory
could have the heuristic potential to suggest avenues of investigation that would
refute it or support it. Finding a null hypothesis with sufficient scope to refute this
nascent synthesis is difficult since there is already general agreement that major
transitions to innovative states have occurred in the past, and it comes down to
refuting their emergent nature, as opposed to their gradual accumulation through
insensible adaptational changes. Major genetic changes can take place outside the
scrutiny of natural selection, and saltatory and critical-point emergences have
occurred during evolutionary history.
The ultimate null hypothesis for an emergence theory would be tested by the
discovery of an environment where evolution by the selectionist definition, changes
in the distribution of alleles, is quite lively, with natural selection firmly in charge, but
with no progress made. When we look at the biological past through narrow windows
of time, this is the kind of stasis we almost invariably observe. Paradoxically, progress
must have occurred, in brief emergent spurts, when we were not looking, otherwise
we would not be here to consider the problem. One obvious truth embraces all of the
Baconian lists and tables. In any physicochemical environment from which a system
that reproduces, duplicates, and differentiates can emerge, all of the above can
happen, has happened, and will happen again, given similar opportunities.
However, before we leave the non-progressive null hypothesis, I should admit that
the first 2 billion years of the history of life on Earth would almost seem to confirm it.
Although I have been writing about the possibility of molecular, epigenetic, and life
cycle emergences on scales of milliseconds, weeks, and months, the emergence of
successful eukaryotic unicells did not occur until 2 billion years after the emergence of
life, and it was almost another billion before successful multicellular organisms
emerged. Little wonder that the benign interference of an Intelligent Designer is so
alluring. What then would an emergence theory usefully have to say about it? Going
back to where we started, there is always the possibility that the global environment
was so homogeneous, and the dynamic stability imposed by the agents of natural
selection so imperturbable, that the first tentative experiments in progressive
evolution were doomed to failure. Maybe that is part of the explanation. Though
experiments might be tried anywhere, they often survive best in stressful places where
competition is low. Those often exist at environmental interfaces. And that is where
symbioses and other associations often emerge. What, then, were the environmental
interfaces when life was first getting to know itself?
Life was traditionally thought to have originated in oxygen-free environments
where there was a concentration of abiogenic organic molecules. A popular current
contender is the high-pressure, sulfurous, marine volcanic vent environment.
Whichever it was (perhaps both), the two kinds of environment probably co-existed,
and between them was a barrier where the pickings were slim for any life forms,
regardless of origin. As to the interface between aquatic and terrestrial conditions, one
was wet, the other dry. And the less challenging interface between marine and
freshwater environments was between the salty and the dilute. The latter was still
stressful enough for unicells, and a long wait for the appropriate generative conditions
to arise is not surprising.
All these environments were anoxic and would stay so until the emergence of pho-
tosynthetic hydrolysis systems. Once those had appeared, the buildup of oxygen to
the point where it would make a difference was certainly on a geological time scale.
Once it did reach that point, two well-defined interfaces came into being. The less
obvious of these was at the fluctuating redox point between oxygenated and anoxic
layers in benthic sediments and water columns. Here there was likely to be congrega-
tion of biochemically different unicells, some with the capacity to detoxify oxygen,
382 Chapter 10
and even to put it to good use. These had the potential to engage in symbioses. As to
the interface between water and the atmosphere: long before the increase in
atmospheric oxygen reached present-day levels, it reached a partial pressure much
higher than is possible for oxygen dissolved in water. Here was a chance for cells and
multicells that could protect themselves from ultraviolet light, and repair the damage
it caused, to get on with the business of making the terrestrial environment more
attractive to a wider assortment of organisms.
Thus did the unlikely become the likely, very slowly at first, but with an accelerat-
ing pace. Through progressive changes in adaptability, higher animals were finally
able to explore new environments and add to their physiological qualities. Those that
behaved consistently and persistently, in relation to each other and to their
environment, accelerated anatomical adaptation. The lack of such adaptability in
primitive unicells contributed to the slow pace of their advancement.
The Magic Formula

We cannot leave the question of how much of a scientific theory emergentism can
provide without asking if there really is a holy grail to be found. To some extent I have
satisfied Stephen Jay Goulds agenda of seeking causes, strengths of causes, levels of
causes, and contingencies, and have added a few more relevant items. I have also tried
to meet the challenge of saying more about the emergent property than that it is
simply the emergent property. (Please dont laugh out loud.) Predictiveness and pre-
dictability, which belong to formal theory, are to some extent manageable, even if we
lack explicit forecasts. Now, what about the greater challenge of constructing a
universal formula that would apply all the way up the ladder of nature, ascending
from emergences in physico-chemical systems, through the emergence of life, to the
emergence of mind? Doyne Farmer (as quoted by Mitchell Waldrop in 1992) usefully
returns us to that question:
Im of the school of thought that life and organization are inexorable . . . just as inexorable as
the increase in entropy. They just seem more fluky because they proceed in fits and starts, and
they build on themselves. Life is a reflection of a much more general phenomenon that Id like
to believe is described by some counterpart of the second law of thermodynamicssome law that
would describe the tendency of matter to organize itself, and that would predict the general
properties of organization wed expect to see in the universe.13
Matter organizing itself? Crystallization meets that requirement. Spontaneous protein

folding does as well. But like the structure and behavior of wet water, they are the
expression of an inherent property of atoms or compounds realized by appropriate
physicochemical conditions. The Second Law of Thermodynamics was once much
discussed by theoretical biologists who attempted to reduce life to thermodynamic
principles. This gave physicists and chemists an opportunity to add their theories
about life, unsullied by its leaky, slimy, stinky messiness. (Scientists, including some
biologists, seem never to have come to terms with living in a human body!) But all
that could be said initially was that living organisms do not defy the Second Law. They
are open (or dissipative) systems that become more complex ontogenically and phy-
logenetically, and in so doing they generate massive amounts of entropy by the
expenditure of useful energy. That life obeys the Second Law says nothing useful that
we did not already know about organisms and their emergent properties.
Fits and starts and an ability to build on what already exists could certainly apply to
cosmological emergences, and obey the principles of quantum and particle physics.
However, a law that would describe the tendency of matter to organize itself would
need corollary laws of emergent reproduction, and the repetitive differentiation of
biological modules. These are emergences that do not happen in non-biological
systems. Further ad hoc laws would then be needed to contain the origin and
development of mind. How these biological properties emerged will not be answered
by physical laws, or by a universal mathematical formula.
Although biological emergences do not defy the laws governing the lower levels,
their causes are usually identifiable only at the transition point. They have new
properties that cannot be assessed before they have arrived. Interesting though a
physical law of the complexification of non-living matter might be, its universality
would fail at the barrier of biological reproduction. That does not write off the
possibility that emergent increase in complexity could be inexorable, and that when
patterns are biological their establishment may be fast and their effects persistent.
Note, however, that th plurals in the Holland quotation at the chapters head
(copies, variants) may indicate some embarrassment with regard to the multiplic-
ity of biological possibilities. Because of the difficulties I have just outlined, I have
been trying to sneak up on a universal formal theory, without expecting to catch it.
Nevertheless the game is afoot. I am at a way station on the quest, coming down the
mountain a few stops back from the summit of biological complexity, while Holland,
Sol, and Goodwin are a few stops on from rigorous simplicity.
In addition to the question of inexorability of complexification, including the
biological kind, there is the question of how many fundamental emergences there
have been during the history of evolution. And can the multiplicity of living examples
be simplified to something approximating a general biological rule? Maybe we need
separate rules for the emergence of life and the emergence of mind, with sexual repro-
duction, endosymbiosis, multicellularity, and other major innovations between the
two. That they are all saltatory complexifications is enough to suggest a universal
patterning, but not a common formula. Some biologists still hope that there can be a
universal theory. Antonio Lima-de-Faria proposed that autonomous complexification
is the result of the organisms physical nature, without much reference to the
prevailing conditions of its life. Thus, he titled his 1988 book Evolution without
384 Chapter 10
Selection: Form and Function by Autoevolution. In the same mode, Stuart Kauffman asked
in The Origins of Order (1993) if there is some principle in physical nature whereby
physicochemical systems must produce an integrated, reproducing biological entity.
There is no question that since the Big Bang the cosmos has become more hetero-
geneous and complex, and has evolved in the old-fashioned sense of unfolding in
time, revealing the potential of its original emergent properties. Even so, it would be
impossible to predict where and when galaxies and their component star systems
would emerge. Farmers organizational equivalent to the Second Law of
Thermodynamics, if formalized, might apply across the non-living board. But
biological evolution, regardless of ideological prejudice, requires biological reproduc-
tion, self-maintenance, and a kind of self-organization unique to living systems.
The Big Bang was the Enormous Emergence, but it was qualitatively different from
the emergence of life. Or am I engaging in a semantic quibble? Has the cosmos
evolved the familiar chemical elements in such a way that certain random combi-
nations such as water and carbon compounds and the rest must arise, stable enough
to hold together, but unstable enough to be pulled apart and brought into more
complex configurations? And have other natural physicochemical experiments
brought them together to reach a critical mass of chemical complexity out of which
life must eventually, if unpredictably, emergethus making us at home in the
universe? This would assuage Kauffmans nostalgia, and if he is right then life is a
consequence of the emergent properties of the Big Bang.
Cosmologists may now start jumping up and down, and shouting Thats what
weve been trying to tell you. But neither metaphysical absolutes nor ontological
assertions about the nature of being have explanatory power. Life has new rules
intrinsic to the emergent properties of reproduction and self-maintenance. And mind,
though a consequence of biological reproduction and differentiation, has a novel set
of rules arising from the unique emergent properties of an expanded and reorganized
brain. The semantic reduction of biological evolution to cosmic evolution is either
delusion or dishonesty.
If cosmologists find their equation, it will say nothing about the higher rules of
biological emergence. To say that life will emerge in a universe that has carbon may
be true, but that it has happened in this instance is not evidence enough to generalize.
To argue that the concept of autoevolution applies generally all the way from the Big
Bang to mind is a variant of the hylozoic (or panpsychic) fallacy. It would imply that
life and mind must somehow be contained in subatomic particles and energies, and
progressive biological evolution must be an unfolding and multiplication of their
initial features. Emergentism saves us from hylozoism. Life and mind are not
properties of the Enormous Emergence, any more than the mammalian neocortex is
embot in the primitive chordate nervous system. As Holland puts it, there are layered
series of emergent patterns, and each has its own novel emergent properties. Each
level may have the propensity to generate the next one up when the appropriate
conditions arise. But the lower layers do not possess the properties of the higher ones.
Kauffman and his associates have devoted a great deal of time to the emergence of
complexity within non-living systems, and find it difficult enough to pin down at that
level, far less in the evolution of organisms. Thus, when John Horgan proclaims the
end of chaoplexity he concludes that complexity theories tend to describe what is
going on rather than to explain them:
Self-organized criticality is not really a theory at all. Like punctuated equilibrium, self-organized
criticality is merely a description, one of many, of the random fluctuations, the noise permeating
nature. By Baks own admission, his model can generate neither specific predictions about nature
nor meaningful insights. What good is it, then?14
The simple answer is that these ideas begin to present alternatives to a prevailing
theory that for seven decades has focused the attention of self-styled evolutionists on
minor, non-evolutionary fluctuations of dynamically stable systems. That theory has
generated no useful predictions about or insights into progressive evolution. It is
armoured against it. The central role that Julian Huxley gave evolutionary progress
has been written out of the neo-Darwinist drama. Instead of predicting the end of
evolutionary biology, Horgan might better ask What good is an evolutionary
biology that ignores the phenomenon it purports to address? And when are we going
to see something that doesnt ignore it? In the meantime, Holland has taken positive
steps toward formal theory, if not toward a single law of organizational evolution.
Even if his material consists only of fragments, they are indeed lawful.15 As he well
understands, their explanation of emergent evolution is limited because they are
modeled on learning novelties in complex systems that were designed by humans.
There is a major leap from here to systems that self-complexify in a manner that is
novel and heritable. Nevertheless, Hollands generalizations, cited at the end of
chapter 8, interdigitate with those I have drawn from the various arenas of evolution-
ary performance. My aphorisms may not be lawful, but they amalgamate the
relevant information, and compare and contrast different points of view, to bring out
relationships or generalities, and reveal exceptions that prove the rules. The generative
levels of emergence, biological or intellectual, need a congruence of all the necessary
parts. So if all of these are put together, how much closer do we get to an integrating
explanation than does the mixed bag of tricks found in the Modern Synthesis? A re-
examination of the construction of the whole is in order.
Layered Series of Generative Procedures

Holland remarks that new wholes emerge through layered series of generative
procedures. This refers to hierarchical dynamic structures whose complexity in real life
and evolution defies a formal theory of evolutionary emergence. To simplify the
386 Chapter 10
problem of identifying the layers of progressive evolution, we can look at them from
two perspectives: historical layering, and the layering of structural grades. Earlier
chapters and sections dealing with the chronology of emergences have given some
idea of the complexity of historical layering, and the fact that it is not entirely
separable from structural gradation. In reviewing them here, geophysiology and the
random impact of contingencies are left out for the sake of simplicity.
The epigenesis of a complex, mature organism from a fertilized egg provides a crude
recapitulatory model of historical layering in evolution. In both development and
evolution, the most visible chronological series of progressive emergences is
anatomical. This, however, is not the most important from the emergentist point of
view, since it can be molded by behavioral changes made possible by physiological
advances. Form follows function, and function follows form. Progressively they
bootstrap each other into the future.
Take vertebrate evolution as an example. The bootstrapping relationship among
behavior, physiology, and anatomy was accompanied by complexification of the
central nervous system and further tuning of the hormonal systemall dependent on
a reliably constant internal milieu. Developmental changes underlying anatomical
evolution involved allometric shifts, hypermorphic additions, and interpolations at
earlier stages in epigenesis, as well as paedomorphic processes. While there were no
radical changes in functional anatomy once a humanoid form was assumed, cranial
expansion, an effective voice box, and dexterous hands were some of the necessary
generative factors accompanying neopallial allometry during the last lap of the course
to humanization. Furthermore, the final structural grade of the cerebral cortex has
added a new layer: acquired mental characteristics that can be inherited through
education. Thus, the historical layers, or hierarchical levels, are internested, and have
effective feedback between them. Novelties are added to early layers as well as to the
top of the pile (not the easiest kind of system to model mathematically), but
progressive evolution requires separation of offices and concurrence of efforts.
The other way of looking at emergent levels is simpler, though more static. It can be
called the hierarchy of structural grades, or a compositional hierarchy (i.e.,
molecules < organelles < cells < tissues < organs < whole organisms < societies < demes
< communities < ecosystems, and so on). The development of a zygote into the hier-
archical modular structure of the early embryo would seem to recapitulate evolution.
Yet that is an oversimplification, since the embryo is a whole at any stage, and its
structural grades mingle, interact, expand, and contract throughout development. As
to the mature whole organism, its hierarchical levels and their regulation are conven-
tionally studied as if they stood alone. And, historically, they have attracted fickle
attention. Once, cellular biology was all the rage; now it is molecular biology. We can
reach an understanding of progressive evolution only by studying them multidimen-
sionally, as wholes moving through time. Though we might tend to concentrate on
the regulation of gene expression as the explanation of evolution of the higher

grades we must remember that gene expression can be altered by changes in the
investment of maternal effects, as the result of behavioral bifurcations, alteration of
external stimuli, internal catalysts, mediator cascade effects, and so on, with genetic
or epigenetic accommodation last if not least.
One implication of Hollands analysis goes beyond the layering I have just
described, being a feature of emergences from the non-living to the mental. Holland
says that once persistent patterns occur they become candidates for combination
with other, persistent patterns (other copies or variants), and that at this point larger
patterns with enhanced persistence and competence can occur. These need not be
vertically layered compositions. Persistent patters may be abiotic coacervates or abiotic
organic chemical films on surfaces. In organisms they may be adjacent holons at the
same focal level. The patterns may be different organisms with a propensity to form
symbioses. Or they may be members of the same species whose interactions change
with population density, reproductive cycle, and season. Interactions also change with
such simple physical rhythms as day and night. Male grizzly bears, for example,
aggressively keep other males at a distance during the day, but in the dark they have
been observed in close, non-aggressive contact.16
Combination of independently evolved persistent patterns occurs only where
generative conditions are appropriate. For example, they have to be in the same place
at the same time if the unlikely is to become the likelyrandomness takes on a
different meaning where the odds are significantly changed. The toss of a coin gives a
50 percent chance of a win, whereas the purchase of a lottery ticket is a long shot. In
the selectionist rulebook, astronomical odds dont matter if there is enough time and
persistent trial-and-error variation. In contrast, the emergentist rulebook considers
how organisms might shorten the evolutionary odds in their own favor. Instead of
treating natural experimentation as random point mutations of DNA that though
heritable might not persist, emergentism provides a holistic synthesis of multidimen-
sional factors. Thus, it meets the demand for a truly interactionist interpretation of
evolution that Susan Oyama calls for in The Ontogeny of Information (1985).
The Holism of Emergentism
Examination of the construction of layered series has brought us back to the dynamic
structure of the whole, which requires examination of the organisms internal rela-
tionships as well as its relationship with its environment, rather than reductionism. In
the genocentric universe, the genes of cats that reproduce most successfully come to
dominate catdom. However, as Jack Cohen and Ian Stewart say in The Collapse of
Chaos (1994), cats eat mice but cat molecules are indifferent to mouse molecules. A
total knowledge of cat and mouse molecules would never allow a prediction about
388 Chapter 10
how mice affect cats behavior, since that has progressed through several emergent
levels. I might add that cats, to successfully pass on their genes, would do just as well
to cosset mice, or simply ensure that the bacteria in their feces were allowed to
reproduce. Cat, mouse, and bacterial genes are much of a muchness; its the
organismal packages that differ distinctively. Nevertheless, reduction is a necessary
tool for identifying causes and mechanisms that participate in emergent evolution,
and systems reduction is valuable for understanding the rules of self-organization.
With the basic emergent properties of life (reproduction, self-maintenance, self-
organization) come repetitive differentiation, and combination. It can be predicted
that nature will experiment, organismal complexity will emerge, and stasis or
equilibrium among existent organisms will be established as numbers rise and
resources become limited. Escape from stasis is made possible by improvement in self-
organizing complexity, expressed as adaptability. This extends the freedom of the
organism from conformity to the environment, and allows some freedom of choice of
behavior, and hence a possible escape route via environmental fringes and interfaces.
The above tenets approach a general biological principle of emergence based upon
the fundamental emergent properties of the first living organisms. These are not
qualities of non-living systems, so they are unashamedly vitalistic, no longer invoking
supernatural entelechies or mysterious black-box powers. This much has been
intuitively obvious to many evolutionary essentialists for at least a century.
Although classical genetics separated the organism from the environment, and the
double helix separated the gene from the organism, they, and the works of modern
molecular biologists and epigeneticists, have contributed to bringing out vitality as a
rational and materialistic emergent evolutionary principle.
Since disequilibration of stasis permits escape from it, and enhances the scope for
further emergences, it is predictable that stress, small accidents, and large catastrophes
will be significant. The nature of some of the particular contingencies likely to be
encountered is unpredictable, and the randomness of natural accidents makes it
impossible to predict what emergents, in what phylogenetic lineages, will survive and
thrive, although adaptability is more reliable than luck.
By asserting the repetitive differentiation of DNA as a fundamental emergent
mechanism, I risk decaying into gene orbit. Of course, the principle applies to
epigenesis and associations too. I must also re-emphasize the axiom that emergences
are the expression of all of the generative conditions of organism and environment as
a whole, and that they result in a constellation of novel properties. Stuart Newman
and Gerd Mller (2000) make the case even more strongly when they argue that the
correlation of an organisms form with its genotype, rather than being a defining
condition of morphological evolution, is a highly derived property. Then they
conclude that genetic change . . . mainly plays a consolidating role, rather than an
innovating one.17
The need for holism (or interactionism) in an emergence synthesis brings us back to
the question of how the whole can be greater than the sum of its parts. I have already
given the example of how the functional properties of quaternary protein structure
constitute a greater whole than the sum of its constituent monomers. At a higher
structural grade, the symbiosis of two different organisms can turn surplus energy and
toxic waste products to mutual benefit. Interactions within societies can alter the
constituent individuals in a variety of ways. Wholeness also resides in the hierarchical
structure of the organism. Each emergent level in the hierarchy has properties to
which the parts contribute, but which do not reside in the parts. Having such an
organization ensures increased efficiency and effectiveness.
One important element of emergence, intrinsic complexification of differentiated
cell types, is overall an exponential function of reproduction and timequite a simple
equation in the absence of natural selection. As a function of the number of differen-
tiated cell types, the curve for all of animal life flattens after the emergence of the
vertebrates.18 But the historical curve of some lineages, especially that of hominids, fits
the simple exponential equation, its logarithmic slope theoretically determined by the
fact that the acceleration of complexification is virtually equivalent to increasing
adaptability and freedom to explore unexploited environments. It could continue to
rise more steeply if we did not voluntarily limit experiments in human genetic
engineering. Looked at more closely, the curve would be seen to be a staircase,
consisting of a number of steep (critical-point) or vertical (saltatory) risers represent-
ing emergent events separated by steps or landings whose breadth is proportional to
the duration of periods of dynamic stability. If the randomness of natural experiments
and accidental contingencies is included, the whole graph becomes irregular, although
the overall shape is not altered.
To express complexification as the increase in the number of differentiated cell types
does not address the final stages of primate evolution. Once a particular cell type, the
neocortical neuron, was acquired, it did not go on to produce variant repeats. The cell
type could of course differentiate ontogenically in the number and topography of
dendrites, in its cell membrane receptors, and in its DNA modifiers. With numerical
increase of neurons, progressive packaging became more important, since each of
those cells had the potential to exchange information with thousands of others. Its
interaction with surrounding glial cells complemented its versatility. Consequently
the whole brain could further differentiate ontogenically to an astronomical degree,
prior to its genetic consolidation (or accommodation). A near infinity of connections
at the level of the individual underlies the emergent quality of the human mind, one
of the other big problems of evolution that emergentism might address. Yet here I
have already fallen into the trap of oversimplification. There is more to mind than
neurons and glial cells with multiple connections and inborn powers of intelligence
and memory. We must not ignore the roles of nutrition, experience, introspection,
390 Chapter 10
education, and social interaction. Ontogenic emergencesbright ideascome when

unusual connections or bisociations are made between cells and brain. Gene-determined
hard wiring would prevent them.
Thus, one generalization about the emergent properties of mind covers the whole
constellation: freedom from fixed action patterns and stereotyped behavior, and
freedom to embrace conventional ways; freedom from competition and predation, and
freedom to challenge them; freedom from conformity, and freedom to conform through
cooperation. Persistent patterns become free to plan and create future patterns.
Emergence as a Dialectical Synthesis
A dialectical synthesis involves bringing together apparently contradictory ideas as

thesis and antithesis so that a new synthesis will emerge. There is a serendipitous
parallel between this interpretation of the history of ideas and the emergence of
novelty from its generative conditions. But beyond this dialectic is the bisociation of
existing facts and ideas that no one had thought of putting together. That is the proper
goal of interdisciplinary research, and from it new concepts sometimes emerge. This is
what Ernst Mayr, without invoking Hegelian or Marxist language, claims for his
version of the Modern Synthesis. But there the contradictions are subsumed under the
thesis, put in black boxes, rejected, or vilified. The reductionism does not resolve
complexity; it destroys it. Emergence does not generate a simple Hegelian synthesis. If
proposed as a theory or a thesis, it already integrates saltation with gradual change,
and the intrinsic with the extrinsic. It is a theory of evolution, which selection theory
is not. Therefore, emergentism rejects natural selection as an evolutionary cause, but
establishes its theoretical importance as a meaningful consequence of emergent
evolution and as a dominating condition of existence.
I close this chapter with a demonstration of how the contradictions of emergentism
and selectionism can, to some extent, be synthesized, and come to the conclusion that
a comprehensive dialectical synthesis cannot be achieved. Therefore, to come to a
dialectical synthesis requires transcending an emergence theory of evolution, to
integrate it with a selection theory of non-evolutionary dynamic stability, and that
task will be undertaken at the beginning of the next chapter.
Summary
The following tables are intended to bring home the Bacon, to outline other general
principles, and expand on the contrasts and comparisons of emergentism provided in
the field trip guide late in chapter 3. In this context, bringing home the Bacon does
not infer the wholesale consumption of the old ham, but only his use of tabulation to
compare and contrast different aspects of nature. Some of the vernacular slogans in
current use are included in brackets. If any have slipped your mind, look down to the
end of this chapter, where they are redefined.
Thesis: evolution by emergence Antithesis: evolution by natural selection
1 Emergence ranges from variation of the Natural selection (defined as differential

existent to large-scale innovation. survival and reproduction) is assumed to
act on small-scale heritable variations.
Commentary
Regardless of the extent of change, large or small, whether at the molecular, organ,
organismal, or population levels, the quality of that change will out. In other words
its outcome will be realized or constrained by how it interacts with the internal and
external environments. If its emergent quality is related to integrity/persistence in
being, it may survive until different conditions arise, when it might then diversify.
2 Emergentism synthesizes intrinsic and Natural selection is most evident in

extrinsic change. Adaptation to relation to extrinsic change, i.e.,
environment is a consequence of adaptation to environment.
organismal changesometimes
behavioraloften set off by the Intrinsic self-adaptations, or co-
environment itself, but also possible as adaptations are tacitly acknowledged, but
autonomous emergence. ignored.
Commentary
The failure of selection theory to incorporate intrinsic change is not entirely a matter
of neglect. But it is unable to logically exclude such change. If molecular and
organismal adaptation is seen to result from the interaction of genes, organisms, and
their behavior in relation to their habitats, some of the apparent contradictions
disappear.
3 Emergentism synthesizes saltatory and By convention, selectionism depends on

gradual change. gradually continuous variation and rejects
saltations.
Commentary
There is no longer any reason to reject the reality of saltatory change. In the case of
critical-point emergence, an appearance of saltation results from the sudden
realization of a potential inherent in a gradually increasing continuity. That might be
assumed to be through adaptational accumulation. Yet the question that remains is
To what extent might continuity of variation be due to an autonomous drive? Here
392 Chapter 10
there might be no convenient accommodation of the emergent and selectionist

positions. Nevertheless, see the next item.
4 Autonomous directional change, or The appearance of orthogenesis is in

orthogenesis, can be equated with self- reality orthoselection of mutations whose
amplifying genetic and epigenetic systems. phenotypic expression is more exaggerated
It may be responsible for much of and therefore more strongly selected than
anatomical divergence. the earlier variation. This apparent trend is
limited by natural selection when it
reaches a point of maladaptation or disin-
tegrity.
Commentary
Self-amplifying autonomous processes occur at the level of codons, larger base
sequences, and possibly epigenetic interrelationships. At present these are in or close
to mainstream evolutionary theory as molecular drive and concerted evolution. For
these, mechanisms have been expounded that are acceptable to all parties. Their
effects can be continuous and rapid, being amplified from generation to generation.
Some are known to be disintegrative, and thereby finally irrelevant to evolution,
needing no supernumerary force to remove them. Self-amplifying processes might also
be stopped before the point of instabilityevery lineage can be shown to have
undergone allometric growth shifts that produced their characteristic anatomies.
Conceptually, orthogenesis gets over the selectionists difficulty in understanding how
the incipient stages of allometric shifts might have sufficient selective value. They do
not require such a value, since the processes are autonomous.
5 There are several generative causal Major causal categories are normalizing
arenas: symbiosis/association; and directional selection acting on DNA
epigenetic/developmental processes; variants.
physiology and behavior.
Commentary
The need to accept saltatory evolution is reinforced when the performances of
generative causes are observed. It is unfortunate that selection theory ignores them
and doubly unfortunate that it does so because they do not fit the theory. Yet its
emphasis on the normalized condition should not be surprising, since dynamic
stability dominates biological history. It thus provides the time for new types to
integrate and fine-tune their innovative qualities.
6 All the previous categories involve real The previous categories are operational at
organisms, and real congregations of them the level of pools of genes in populations.
interacting within their demes as well as This requires the working hypothesis of an
interacting with similar groups of other external causal agentnatural selection.
species in communities.
Commentary
Here I must admit that it is difficult to integrate reductionist population thinking.
However, populations are theoretically and practically significant. For me to abandon
their reality at this juncture would be as anti-intellectual as the populationists eviscer-
ation of real populations to turn them into gene pools. Once the population has been
re-invented as an interbreeding assemblage of organisms in a real environment, the
problems disappear. The integrating qualities and behaviors of such populations are
offset by geographical limitations. Under limiting, stressful conditions, they are
vulnerable to disequilibration. Thus, periods of equilibrium that lead to expansion in
space and time reach thresholds where population bifurcation is possible. This
parallels in space the temporal epigenetic conditions of alternating stable growth and
expansion, punctuated by unstable interphenes where developmental bifurcations are
possible.
7 Genetic assimilation results from the A metaphorical external agent, selection

consistent and persistent behavior of pressure, is adduced to explain the
individual organisms. Appropriate generation of genetic changes appropriate
molecular experiments are then incorpo- to the prevailing conditions of life.
rated. Phenotypic form and function
precede genotypic changes.
Commentary
There was never much of a logical difference between Lamarcks organisms-
responding-to-needs and the Darwinists evolution-responding-to-selection-pressures.
But Lamarck came closer to the truth by putting the organism, rather than the gene
pool, on the line. The behavior of the organism determines what is adaptive. Whether
we say that it constrains the viability of natural experiments or that it changes the
selection pressure, it comes down to the same thing: What the individual organism
does is important in the evolutionary scheme.
8 In all of the causal arenas, saltatory Selection theory considers saltatory change
emergences may occur. Both saltatory and to be detrimental, and to diminish the
critical-point emergences may be sufficient causal role of natural selection acting on
to escape existing dynamic stability gradual change or imperceptible variation.
394 Chapter 10
Commentary
This revisits items 3 and 5 above. But what may be added is the realization that differ-
ential survival and reproduction are normally present, whether or not change is
saltatory or gradual. Whichever it might be, the experimental quality is worked out in
relation to the life and environment of its organismal possessor. This does not confirm
the inference that the working out of those qualities in environments is evolutionar-
ily causal, nor that natural selection, despite its ubiquity, is creative.
9 All of the above items are correlated Environmental change alters selection
with environmental change and the pressures.
response of organisms to such change,
both ontogenic, and by genetic, epigenetic
and physiological accommodation.
Commentary
In this case the selectionist antithesis is speciousmetaphorical forces need no logical
synthesis. The real and positive qualities outlined in item 8 are self-sufficient. Much as
it might so proclaim, and much as its reluctant brides might close their eyes, selection
theory has no droit de seigneur over genetics and molecular biology.
10 The potential for emergence resides in Natural selection, qua differential survival
the primary qualities of life: simple and reproduction, created the primary
persistence through reproduction, self- qualities of life through the preservation
maintenance, and self-organization. of persistent systems.
Commentary
Competition is an effect of emergent qualities once their possessors have sufficiently
increased in number to make resources limiting. Natural selection is the outcome of
competitive interactions. The result is that certain emergent qualities, whether simple
adaptational gene mutations, or physiological/behavioral adaptabilities may come to
dominate certain populations. Although competition and natural selection are
realities, they are not creative, but are the consequences of creative natural
experiments.
11 Intrinsic complexity is increased by Complexity is a coincidental consequence

multiplying and integrating the of the accumulation of adaptations.
fundamental genetic, epigenetic, physio-
logical and morphological units of
organisms.
Commentary
Theoretically, biological self-organizing systems (i.e., those that involve reproduction)
will increase in complexity and integrity without reference to external conditions.
Integrity infers a degree of autonomous regulation that could be loosely described as
internal adaptation. The modification of these integrated qualities may be randomly
generated from existing modules, but their persistence is proportional to their
integrative qualities. There is nothing of random aggregation in this process. All
organisms inhabit environments, and modifications that are perceived as adaptations-
to-environment are consequences of the adaptability of well-integrated wholes that
allows their entry into and survival in new habitats.
12 Complexity is further increased by dif- Natural selection favors complexity and

ferentiation and reorganization of the adaptability when they have high fitness.
multiple unitsmolecules, cells, organs,
organisms. (Mixing and matching. It favors regression and simplification
Separation of offices and concurrence of when those have high fitness.
efforts. Repetitive differentiation.)
Commentary
Complexification through multiplication of subunits as presented under thesis 11 is
an oversimplification, since biological versatility depends upon differentiation as well.
Differentiation, in turn, is ineffective, unless its products are regulated. Therefore a
multiplicity of epigenetic and physiological processes need to interact simultaneously.
This is one of the relatively unknown factors of emergent evolution. The selectionist
antithesis is correct as far as it goes. Yet it reinforces the realization that much of the
time complexity and adaptability do not have high fitness, although their emergence
will out, regardless of their ultimate fate. The reverse of the coin is simplification and
regression, which happens under prolonged conditions of dynamic stability. (Marine
fish lose the ability to return to fresh water and vice versa.) I will not press the point,
but this kind of evolution-by-natural-selection strikes me as more akin to devolution.
13 Generative conditions for emergences Key innovations are caused by selection

are strong at environmental interfaces pressure, which is strong at environmental
where there is opportunity for novel interfaces.
organismal associations. (More mixing and
matching. Being in the same place at the
same time.)
Commentary
Here there is no fundamental contradiction between thesis and antithesis. Both accept
that evolutionary conditions change at environmental interfaces. Selection pressure
396 Chapter 10
under these circumstances is actually a release from the pressure of normalizing

selection.
14 At environmental interfaces there are Environments act as filters that remove

opportunities and benefits for escape from incompetent variants.
old environments and their stases.
Commentary
Here again there is no serious conflict. It is, however, more to the point to appreciate
the positive emergent qualities of natural experiments than to emphasize the negative
qualities of variants that fail.
15 Critical-point emergences find an Epigenetic metamorphoses are no more

analogy with ontogenic changes at than selectively advantageous accelera-
epigenetic thresholds. Saltatory bifurcations of changes that previously followed a
tions are also possible at these nodes. path of gradual continuity.
Commentary
Without argument, epigenetic alternatives must sink or swim according to prevailing
internal and external conditions. But they are implicitly subject to loose canalization
and may have no initial gene determination. That too will pass, so that ultimately the
alternatives will often be found to have become tightly genetically assimilated or
canalized. The concept of selection pressure as a constraining or creative influence is
superfluous.
16 Populations reach density thresholds. Population-density effects are gene

There they may be limited to fluctuation determined and selectable.
around the point of carrying capacity. But
physiological and behavioral alternatives
that affect populations en masse may crop
up.
Commentary
In response to population-density stress, entire demes may remove themselves
(starving locusts becoming flying swarms). Only epigenetic exceptionsflyers
would be involved in the first instance, but at that point they would then constitute
an innovative lineage, removed from the parent population. And all members of the
new population would have that quality. The stress response might be an expression
of atavistic traits or epigenetic novelty that has no fixed DNA determinant. Either way,
the standard explanations of allele concentrations at the peaks of genetic landscapes
are inadequate.
17 Adaptable organisms may concentrate The organism changes the selection

activities in a particular behavioral and pressures.
environmental direction. This determines
the adaptiveness of subsequent genetic
experiments (organism driven).
Commentary
This thesis restores the participation of the organism in its evolutionary future. Neo-
Darwinism reduced the organism to an ephemeral bag of alleles. Yet the antithesis that
the organism can change selection pressures is already close enough to the thesis that
physiology and behavior of the individual can lead to genetic assimilation and diver-
sification.
18 The study of evolution is the study of The study of evolution is the study of the
the generation of emergent properties. numerical distribution of traits in
populations.
Commentary
This is not too difficult. The study of evolution is indeed the study of emergent
properties. The study of the numerical distribution of traits in populations is also the
study of emergent properties. However, the latter case is limited to the prevailing
ecological conditions. What we need to integrate are changes in the prevailing
ecological, developmental, physiological, and associative conditions. And we also
need to rethink the meaning of adaptiveness in the context of emergence.
19 Adaptiveness is synonymous with The natural selection of adaptiveness is the

emergent property and the integrity of essence of evolution.
the whole organism. It does not require
metaphorical assistance.
Commentary
Along with several earlier articles, this final one returns us to matters of biological
advantage, usefulness, and adaptiveness and how they can be synthesized with
self-organization (both in development and in the operation of regulatory systems in
the matured organism), self-maintenance (molecular repair, tissue regeneration, and
homeostasis at cellular and whole organisms levels), emergent properties that make
wholes greater than the sums of their parts, and those that have lesser roles in survival
and reproduction. So! says the selectionist. You mean new traits that enhance
survival and reproduction, and so are spread throughout the population by natural
selection. I am indeed talking about certain new traits that enhance survival and
398 Chapter 10
reproduction and do indeed spread throughout the populationunder certain

ecological circumstances. But I am not forgetting that the qualities of those new traits
came into being with them, not as value added by natural selection. And I am
remembering emergent adaptabilities that may not be called into immediate use, but
have a potential to be advantageous under contingencies that often involve the
diminution of the agents of natural selection, such as competition and predation.
Structures and functions that were already integrated gave rise to those adaptabilities,
and they, in turn, made the whole organism even greater than the sum of its parts.
In conclusion, it should be clear that some of the selectionist antitheses presented
here are irreconcilable with an emergence thesis of evolution. The potential for a
synthesis is improved by the realization that consequent to major emergences, adap-
tational diversifications, are genuine evolutionary changes that are part of the
re-equilibration process. Adaptive radiation is variations on a theme, rather than
progressive complexifications. Yet it too relies largely on minor emergences. The
remaining question about this adaptive diversification is: to what extent does it
depend on orthogenesis by self-amplifying mechanisms, or the more conventional
process of random change accumulated by natural selection? Since the final
dynamic equilibrium usually involves an inescapable degree of specialization, adapta-
tional evolution peters out. Therefore emergent, progressive evolution can only be
dialectically synthesized with the equilibrium state and the selection syndrome above
the level of evolution, as a synthesis of biology, which is the subject of the final chapter.
Definitions of Terms Used in Tables
Being in the same place at the same time Points to generative conditions where the
probability of emergent novelty is highwhere the unlikely has become the likely. See
also mixing and matching.
Constellation of emergent qualities Emergences often have multifunctional conse-

quences. Only one may be immediately advantageous, but the others represent a
potential for diversification or evolvability.
Critical-point emergence In a continuous series of changes a new or enhanced function

may appear in the manner of a saltation (e.g., wing enlarges to point where lift exceeds
drag and gravitygliding to true flight).
Generative conditions (in chemistry, physics and cosmology: initial conditions) The
combination of circumstances that contribute to an emergence.
Genetic assimilation Phenotypic changes induced by the behavior of the organism in

relation to its environment become genetically fixed, wherever genes exist that can
mimic the effect, or wherever the genome can proffer experimental innovations that
might match. Thus the organism determines what is adaptive, and phenotypic change
adds to organismal quality. Some of these effects involve complexification through
self-organization, i.e., through non-DNA epigenetic assimilations.
Geophysiology Organisms affect the environment directly (e.g., produce atmospheric

oxygen by photosynthesis), and organisms contribute to biospheric equilibria
(affecting climatic cycles and changes etc.)
La vie libre Bernards expression for the independence of life afforded by homeostasis.
Mixing and matching Organisms that congregate with others of different species in
particular environments may interact epigenetically or symbiotically. Successful
symbiotic and sexual associations are those that match well, by complementing each
others qualities. Mixing and matching also applies to natural experiments with DNA
exons and protein domains.
Persistence in being The Darwinian term for survival through innate flexibility of con-
stitution (i.e., through adaptability/homeostasis).
Physiogenesis The environment directly imposes physicochemical change on the

organism; e.g., the environment cools, the organism cools.
Repetitive differentiation Holons (modules) at the molecular, organ, and organismal

levels are duplicated, reduplicated, and differentiatednatural experiments that
increase adaptability (Aristotles separation of offices and concurrence of efforts).
Saltatory emergence Sudden large-scale change that is rapidly manifested on an

organismal time scale (e.g., all-or-nothing establishment of proto-mitochondrial
prokaryotes as endosymbionts in eukaryotic cells; deviations in early epigenesis).
The unlikely becomes the likely Hollands shorthand for heterogeneous distributions of
persistent patterns that have the potential to interact and to become more complex
and therefore more persistent.
Use it or lose it Regression is a common process that need not be detrimental, even as
overall organization increases. Sometimes it redefines a particular way of life. Some
labile biochemical pathways may be redirected by the loss of a particular enzyme. But
the genetic machinery may remain dormant, to be revived later.
11
A Biological Synthesis
Taking the route you would be likely to take

From the place you would be likely to come from
. . . What you thought you came for
Is only a shell, a husk of meaning
From which the purpose breaks only when it is fulfilled
If at all. Either you had no purpose
Or the purpose is beyond the end you figured
And is altered in fulfillment
T. S. Eliot, 19431
These lines from Eliots poem Little Gidding are particularly apt to my pilgrimage to
this point. The figured end was not a synthesis of biology. First, my route pointed to
the replacement of selection theory with an emergence theory. Then I tried for a
synthesis of the two. In the previous chapter, I set out a table of contrasts between
emergence theses and selectionist antitheses, intending to integrate the contradic-
tions, to produce an Emergence Synthesis of Evolution. It is a near-impossible task,
since the emergence thesis deals with the major mechanisms and processes of evolu-
tionary change, while the selection antithesis deals largely with non-evolutionary
fluctuations in the demographics and ecology of populations. The Modern Synthesis
solves this problem by fiat: stasis is evolution. However, selectionism cannot be
dialectically synthesized with emergentism within evolutionary theory any more than
apples can be synthesized with oranges. They are both legitimate yet separate
categories of biology, dealing with different phenomena. A synthesis of an emergence
thesis and a selectionist antithesis can only be achieved at a higher dialectical level,
namely life itself, in the form of a biological synthesis. To be more specific, it is a
synthesis of lifes history in both its evolutionary and static phases.
If readers were to start this book at the final chapternot unusual among bookstore
browsersthey might wonder what such a synthesis might mean, and why such a
402 Chapter 11
thing should be necessary. It is necessary because understanding the history of life

needs both the component of evolution, which involves discontinuous, complexifica-
tion on a biological time scale, and the component of dynamic stability (i.e., the
selection syndrome), which has dominated the history of life on a geological time scale.
It is necessary to see the two components as different from one another, and that
emergent evolution results in new phases of diversification and dynamic stability. It is
necessary to end selectionisms claim to all evolutionary change, and to disestablish
the Modern Synthesis. This then is my purpose breaking only as it is fulfilled.
My particular synthesis of biology is not original. It has historical roots in Lamarck,
who saw the importance of progressive evolution, emphasized the individual
organism, and suspected that adaptation to environment was a disruption of evolu-
tionary gradation. Its historical roots in Darwin are weaker, since he did not know how
to deal with the evolution of the lower to the higher, denied the saltatory nature
of emergent evolution, addressed mainly the processes of dynamic stability, and
elevated natural selection to the status of a secular creator. His critic St. George Jackson
Mivart was much closer to an evolutionary synthesis of life. His sense of the history of
life as a series of intermittent equilibria and disequilibria was combined with a proto-
structuralistic mechanism of autonomous progress. Much of the theorizing of Mivarts
contemporaries, the neo-Lamarckists, was also relevant to a biological synthesis.
Curiously, the form given the Modern Synthesis by its British founder, Julian
Huxley, was originally close to a theory of biology. Its goal was to understand evolu-
tionary progress, by amalgamating as many biological subdisciplines relevant to
evolution as possible. However, his version succumbed to the mathematical neo-
Darwinists and evolutionary ecologists. The American version, which opposed the
very idea of evolutionary progress, was never a comprehensive synthesis in the first
place, and was little more than genetics and population biology in an ecological
context.
Thirty years ago I was assaulted by a book title during an innocent visit to the library
stacks of Glasgow University. It was Space, Time, Form: The Biological Synthesis,
published in 1962 by the gadfly evolutionist Lon Croizat. And it came close to a
synthesis of biological history. Its major theme is the diversification of evolutionary
lineages in relation to biogeographical changes, but Croizat understood the
importance of the progressive evolution of adaptability, and also proposed
mechanisms of orthogenesis. The evolutionist Gareth Nelson, also much intrigued by
Croizat, proposed a theory of comparative biology that also came at the central
problem from the periphery of diversification (Nelson, 1970).
My present perception of a synthesis of biology has a thematic commonality with
Niles Eldredge and Stephen Jay Goulds punctuated equilibrium. Theirs was, however,
closer to the mainstream of evolutionism. They proposed that speciation was
relatively rapid, and was followed by a long phase of dynamic equilibrium until the
A Biological Synthesis 403
species perhaps became extinct, or again rapidly bifurcated. The concept was flawed in
that it erroneously emphasized speciation as a pivotal process of evolution, and did
not adequately explain the processes of change, which, moreover, operate at higher
speeds than they suggested. Furthermore, instead of following through, both authors
took a defensive stance in the face of strong selectionist opposition, and apparently
decided to opt for respectability over revolution. In an essay co-authored with
Elisabeth Vrba, Eldredge also wrote: A general theory of biology is a theory of hierar-
chical levelshow they arise and interact.2 This is equivalent to my argument that
new hierarchical levels are emergences; their interaction within the organism is the
ground of adaptability, though influencing and influenced by the external
environment. Later in this chapter, I will return to the vexing issue of speciation as an
evolutionary event, since it is relevant both to emergentism and selectionism.
A comprehensive synthesis of biology would be required to explain the origin of life,
as well as its hierarchical composition and subsequent history. That origin was
certainly a grand emergence, if not a set of multiple emergences. But the analysis of
emergent evolution provided in the previous chapters deals with organisms that are
capable of reproduction. However much it might hint at the possibilities, it is insuffi-
cient to explain the origin of biological reproduction from non-living generative
conditions. Therefore it falls short of the requirements of a complete synthesis.
Nevertheless, it has a strong dialectical component in its integration of emergent
evolution with stasis. It asserts that life has followed an irregular pattern of rapid evo-
lutionary advances in complexity and adaptability. Where the agents of natural
selection are diminished or absent, major emergences have undergone diversification,
which has a component of non-progressive minor emergences combined with adapta-
tional change. The latter becomes canalized into specialization, and the conditions are
now set for extensive phases of dynamic equilibrium. For convenience, the two
components of change and equilibrium are temporarily isolated and their processes
set out; evolution first:
Progress means an increase in complexity, which equates with improved self-organ-

ization and greater adaptability.
Emergent evolution may be saltatory, or it may spontaneously occur at critical

points, or thresholds, in continuous processes.
There are both extrinsic and intrinsic causes of emergent evolution.
Natural experiments in evolutionary change can occur randomly and non-

randomly at any time where the generative conditions exist, but they are resisted by
existent equilibria.
404 Chapter 11
Natural experiments in evolutionary change are rapid in a time scale of microsec-

onds for biological molecules, seconds for physiological changes, hours for behavioral
changes, days to months for epigenetic changes. If these changes are not resisted by
existing dynamic equilibria, emergent organisms can undergo adaptive diversification.
Major emergences increase adaptability by having multifunctional features.
Resistance to change can be overcome by emergent innovations that are

immediately more successful than the qualities of organisms that are part of the
existent equilibria.
Resistance to change is avoidable by innovative, adaptable emergences that can

range more widely and find environments where resources are favorable, and where
predation/browsing is low.
Resistance to change can be removed by the catastrophic disequilibration of existent

stabilities. Here, adaptability is at a premium.
The removal of existent stabilities allows diversification of innovative organisms

that were previously obstructed.
Progressive emergent evolution in animals means greater freedom to choose how

and when to act. That animals should have such greater freedom increases their
individual roles in generating further evolutionary change.
Next, the nature of ecostases (dynamic ecological equilibria) that have dominated the
history of life:
Equilibria may be organismal (i.e., physiological) or ecological (involving behavior,

the physicochemical environment, and intraspecific and interspecific relationships).
Organismal equilibria, such as cellular and organismal homeostasis and

homeorhesis, resist change but can be disequlibrated, usually by external conditions.
Ecostasis is reached when the interactions of organisms in their environment result

in only minor fluctuations of allele and species distribution.
Adaptation to and specialization for environment, within species and genera,

increase the diversity of species, and strengthens the final state of dynamic
equilibrium. Adaptation and specialization are therefore components of diversifying
evolution that straddles the emergence thesis and the selection antithesis. Diversifying
evolution is emergent evolution but has the consequence of ecostasis.
A change-resistant ecostasis can be disequilibrated by a large-scale emergent evolu-

tionary change in one of its interacting species, or by the emergence of a new type.
Catastrophic disequilibration of ecostasis is more likely and more effective than the
previous cause. It allows diversification and regrouping of the more innovative and
adaptable types, which finally reach a novel equilibrium that will persist until a suffi-
ciently disequilibrating cause occurs once again.
As was noted in the introduction to this chapter, the biological synthesis contains
both the component of progressive evolution, which involves discontinuous, com-
plexification on a biological time scale, and the component of dynamic stability (i.e.,
the selection syndrome), which has dominated the history of life on a geological time
scale. It proposes that the two components are different from one another, and that
emergent evolution results in a slower phase of diversification with both emergentist
and adaptationist implications, and finally long phases of dynamic stability. To give
the synthesis a more distinct character, I propose that selectionisms claim to all evo-
lutionary change be dropped. To help disestablish the Modern Synthesis, what follows
emphasizes the distinction between emergent causes and selection effects. To be
candid, rather than leave neo-Darwinist population biologists entirely in peace, I
would advise them to get rid of the expressions natural selection and selection
pressure altogether, and find ways to express themselves without archaic, jejune
metaphors.
What Difference Does It Make?
What of it? What difference does it make? cried Herbert Spencer Jennings in 1927,
when biological emergentism was a current Idol of the Theatre.3 He hoped that one
purpose would be the escape of biology from the domination of reductionism, by
demonstrating that new emergent levels have irreducible novel properties. Biologists
who thought evolution was progress from lower to higher might be rescued from
accusations of anthropocentrism. Faint hopes; such criticisms are still heard from con-
ventional evolutionists, and reductionism rides tall in its journey to the empty shell
of ultra-Darwinism.
A higher synthesis will integrate an emergent evolutionary thesis with the classical
neo-Darwinist antithesis, recognizing that their complementarity clarifies the history
of life. The big difference is that evolution has been removed from the neo-Darwinists
Modern Synthesis and natural selection is no longer considered to have any causal
406 Chapter 11
validity for evolution. We have barely scraped the surface of the study of emergent
evolution, so there is plenty of scope within the theory to proceed in the major causal
arenas of symbiosis/association; physiology/behavior and development. If these are
not taken to be trivial proximate causes, with natural selection as the governing
ultimate cause, some intellectual progress is inevitable.
The major goal of biological emergentism is to understand progressive evolution.
Maybe I should take this final opportunity to emphasize that by progressive evolution
I mean increase in complexity. And complexity is not simply a multiplicity of parts,
but an effective ordering of the parts through self-organization. By self-organization I
infer the interactivity of the parts that arranges them in a hierarchical dynamic
structure and also maintains itthe way a single-cell human zygote does, on its way
to becoming and being a person. There doesnt have to be an increase in the total
number of parts nor the total number of differentiated cell types to achieve greater
self-organization, though some such correlations do exist. Progressive evolution is
characterized by improved physiological and behavioral attributes. The consequent
freedom of choice and action has a feedback effect on both developing and mature
anatomy.
Symbioses were major emergences en route to the origin of eukaryotes. Sexual asso-
ciations and cellular differentiations were major emergences en route to the evolution
of complex multicellular organisms. Social interactions also had feedback effects on
behavior and physiology. And the organismal whole was influenced by environmen-
tal changes. Some resulted from biological activity that oxygenated the biosphere.
Some came through the invasion of new environments. Some came out of unpre-
dictable environmental contingencies: continental drift, volcanic catastrophes, bolide
impacts, and wobbles in the tilt of Earths axis, along with severe climate changes.
Contingencies or not, progressive evolution was inevitable in some evolutionary lines,
because of the generative potential of the first living organisms. Therefore, Lamarck
was not altogether wrong in his progressionism. These generalizations are not limited
to animals, but affect the other kingdoms, such as the plants, to a lesser degree.
Now that I have recapped the previous ten chapters in a single paragraph, back to
my original purpose of linking progressive evolution and emergentism. To establish
that link, I had first to shift your attention from demographics to the generation of
changefrom natural selection to variation. If you had felt that the random identifi-
cation of adaptive traits through the quantification of fitness was enough, I had to
persuade you to consider the more direct approach: the comprehensive examination
of emergent novelty and an assessment of its place in the evolution of organismal
wholes. When that was achieved it became possible to return to the syndrome of
natural selection, as the establishment of prolonged periods of dynamic stability. Then
it could be reintegrated with emergence in the biological synthesis. Without such a
regrouping, the current quest for genes for everything, in order to validate a
nineteenth-century superstition, would continue to make a mockery of biology.
Furthermore, it had to be appreciated that no emergent hierarchical level, from gene

to society, is more important than any other. Those who figure that the end of evolu-
tionary biology will be nigh when weve sorted out the proteins as well as the genes,
must transcend that delusion too, and realize we will still be scratching the surface.
The pundits who have pronounced the end of evolutionary biology are themselves
finished. The rest of us have an exciting future of new ideas and new discoveries. That
is how emergentism can gain fulfillment. The new purpose that transcends that
figured end is a synthesis of biology.
In Agnes Arbers seminal work on the philosophy of biology, The Mind and the Eye
(1954), she notes how the mind can apply different ways of seeing the same evidence,
a theme adopted by the structuralists A. J. Hughes and David Lambert (1984). It is a
different way of seeing to observe the genesis of evolutionary novelty, as opposed to
its fate. The clay of life periodically, autonomously, and spontaneously emerges to
more complex levels. When generative conditions are right, a pot is produceda
thing in itself; there is no magic potter for it to turn against, as the Darwinist E. B.
Poulton objected. The market may find it wanting, of low value, and reject it; but that
affects neither the pot, nor its intrinsic nature, nor its origin, nor even its continued
production. A different perception of natural selection is necessary for a new outlook.
Another purpose of emergentism is to boost out of the genocentric universe to one
populated by real organisms.
Ultra-Darwinism, in combination with reductionism and media hyperbole, has
polarized modern biology, the social sciences, and public opinion. May we now ask
what difference it would make if natural selection were seen as a consequence of, and
subsequently an obstacle to, evolution, not as its cause? How then would diversifica-
tion be explained, and where would speciation fit into the new scheme? What
difference would it make to biology in general if an emergence theory of evolution
were accepted? What difference is there between futures predicted on the basis of neo-
Darwinism and emergentism? What difference would it make to chemistry, physics,
and cosmology; or, going the other way, to anthropology, psychology, sociology, and
economics? Does it suggest why humans do what they do? What difference does it
make to ontology, and to the gulf between quality and quantity and that between sub-
jectivity and objectivity?
Natural Selection as a Barrier to Evolution?
What if, without prejudging alternatives, natural selection were better understood as
the hypostasis (or imposer) of dynamic stability? That is how selectionists actually see
it, when they open their eyes. The conventional journey has already taken us close to
that vista since normalizing selection and stable evolutionary strategies are the most
common conditions. The exception, directional selection, may only be the
408 Chapter 11
consequence of autonomous amplifications and epigenetic constraints. The reverse of

the question is more important: what might be biologically possible in the absence of
the agents of natural selection?
There is no longer any heresy in the notion that the Eden of life was a natural
laboratory where a warm dilute incubating medium could have been seasoned with
organic spices from outer space, or that it could have been a pressure-cooked Hadean
brew of sulfur and seawater. But, before all, it was vacant. Emerging founders were free
to experiment with all possible variations that met the primary qualifications of
integrity and reproduction. They increased in number and experimented further
without impediment, until they saturated the available space and ran short of
resources. The obstacle of natural selection was encountered for the first time when
they began to compete with each other and prey on each other. Freewheeling experi-
mentation was not terminated. But at that point the only experiments that enjoyed
immediate success were those that adjusted organisms to existing dynamic equilibria
of the environment and their own inner coordinative conditions.
Thereafter, only the rare experiment could transcend the hypostasis of natural
selection to re-enter Eden. Sometimes the laboratory itself was reconstructed, as when
the biosphere was oxygenated. Sometimes a random catastrophe cleared the bench to
allow the survivors to try out their own new experiments. Sometimes adaptable
emergents moved to a brand-new environment, from sea to fresh water and then to
land. However, where environmental change was gradual, natural selection continued
to resist evolutionary experiments. Although dramatic demographic shifts might have
occurred, they involved existent forms, except on rare occasions when novel
emergents had such radically improved or novel features that the old competition
ceased to matter.
Natural selectionism, reductionism, population thinking, selfish-gene-ism, ultra-
Darwinism, scientific journalism, and fear of the unknown demand that the
universe be comfortably simple, and therefore genocentric, if not merely molecular.
Thus, it would take the full perception of natural selection as a barrier to evolution,
and appreciation of the generative evolutionary processes of emergence, to shift to a
holistic universe, where organisms are recognized as real entities that internally order
the action of their genes and externally respond to the outer environment, as well as
changing it on occasion.
Nevertheless, a synthesis of biology must retain an understanding of stable
equilibria in populations and species, and so identify the value of conventional
population genetics and ecology, devoid of the logical and polemical excesses of the
old selectionism and ultra-Darwinism. Here is a brief example of what is right and
wrong about current interpretations of neo-Darwinism. The following came in 2001
from an editor of Science, commenting on an original article in the American Naturalist
(once the organ of American neo-Lamarckism); its authors are not responsible for what
the reviewer writes:
Natural selection is the pervasive force shaping the evolution of living organisms. Selection can
take several formsdirectional, stabilizing, disruptive, indirectand can act in different ways on
different organismal traits.
In recent decades much research has been devoted to measuring the strength of the various
types of selection on phenotypes and quantitative traits both in the wild and in the laboratory.
Kingsolver et al. [2001] analyze this literature and uncover some unexpected patterns. In both
vertebrates and plants, the strength of selection on morphological traits was twice as great as on
life-history traits. Strength of selection on some components of fitness, such as fecundity or
mating success was greater than on others such as survival; the strength and frequency of
stabilizing selection, which keeps a trait constant, was no greater than that of disruptive
selections. This synthesis provides a fresh view of the complexities of the evolutionary landscape
and of the statistical hurdles that need to be cleared.4
Pervasive, shape-shifting, and versatile, the ghost is still in the machinethe magic
potter is still throwing the pots. And revelation will come out of a bigger computer
with a better stats package. Apples are compared with oranges, though some fruits,
such as physiology and behavior, are still forbidden. Well, maybe survival as opposed
to fecundity has something to do with physiological adaptability, and its usually the
specialists that are numerically superior to the generalists. To be fair, Kingsolver and
his colleagues usefully tested common assumptions of neo-Darwinismfor example,
that normalizing selection should be more common than disruptive or catastrophic
selection. It isnt. But its an exception that proves my rule. The dynamic stability that
usually predominates in an ecosystem does not have to be homogeneous. In the
classical case of disruptive selection, the various color morphs of the escargot Cepaea
nemoralis are adapted to microenvironments where there might be dark woodland,
open heath, short grass, clumped rushes, and hedgerows. So the population shakes
down into a mosaic of different morphs living in appropriate conditionsassuming
that there is strict genetic determination of the morphs, and not a large ecophenotypic
component, which is always possible. Despite the disruptive epithet, it is merely a
lumpy dynamic stability.
As to stronger selection for anatomy than life-history traits, there is a lot of environ-
mentally sensitive flexibility (or broad reaction norms), even in strongly canalized
morphogenesis, so the two cannot be arbitrarily separated. The rarity of directional
selection reinforces my argument that natural selectionqua ecostasispowerfully
resists innovation. I am oversimplifying, but should not need to remind you tenacious
readers that natural selection does not prevent evolution. Natural experiments in gene
mutation, and in more complex arrangements, occur all the time, where the
generative conditions are suitable. Natural selection blocks these innovations from
demographic significance. If they show progressive improvements in adaptability,
they may persist, but their numbers may not increase sufficiently to flag them with
superior selection coefficients. This re-emphasizes how selectionists look at the adap-
tational distribution of alleles in abstract populations. These gene pools dont really
410 Chapter 11
exist in real environments that are home to real organisms in an entangled bank of
physicochemical and biotic conditions. Such analyses and comparisons give an
indirect measure of the emergent qualities of organisms under the prevailing
conditions of competition or cooperationi.e., interaction. When those change, a
different feature may be found to be the best adaptation. In the meantime, one of
the common results of competition is regression, not progressive evolution. Another
epistemological caution should be raised in this discussion. Kingsolver and his
colleagues have tested unwarranted assumptions and taken a broader comparative
view of what they take to be the mechanisms of evolution. If they were to meet the
real challengetesting the fundamental assumption that natural selection is an evo-
lutionary causethey could really shake the scales from their readers eyes.
Here is another exercise in translating from selectionspeak to a more objective
language. In Making Sense of Life (2002), Evelyn Fox Keller attributes the following
aphorism to Garrett Odell: Robust gene networks are the only networks natural
selection can evolve.5 I have already (in chapter 5) remarked positively on the value
of Odells models for demonstrating how whole network systems have emergent
qualities that are not found in the parts. That is not in dispute. But what does the
aphorism mean to you, or to Keller and Odell? The sense is that robust networks are
the only kind that can persist in fluctuating environments; in other words they are
adaptable. But that property comes at the point of origin of the system, not as the
subsequent effect of a metaphorical force that somehow metamorphoses into a
mechanistic cause. Odell and his colleagues deal with system flexibility in a way that
makes ad hoc figurative language unnecessary. So putting it back again is counterpro-
ductive.
The Barrier of Natural Selection and the Rate of Evolution

I have made it clear in earlier chapters that emergent evolution is rapid. Looking
through a narrow window in time shows us molecular events occurring in microsec-
onds; physiological changes taking milliseconds, hours, or perhaps days; and
epigenetic experiments being field tested in days to months. Speciation might take
years, but since that is not a pivotal aspect of evolution, maybe simply a slow
consequence of emergent evolution, I do not count it seriously (q.v. below). In the
absence of the agents of natural selection the continued diversification of natural
experiments that preserve the integrity of the organism would potentially occur on a
limited, biological time scale.
In contrast to the emergentist view, the selectionist looks at the length of time taken
from the origin of life to the present time, and that involves a geological time scale of
several billion years. This concept of evolutionary time has led to the averaging of the
natural selection of random point mutations to create potentially misleading
molecular clocks. Where the paleontological evidence doesnt fit, molecular biologists
complain about the tyranny of the fossil record. They need to accommodate the
knowledge that molecular change is not only instantaneous but clustered, especially
in the wake of large-scale genomic changes in the form of sequence repetitions, gene
duplications, and chromosome and whole genome duplications. Then they need to
subtract the long periods of dynamic stasis, when, even if molecular and organismal
experiments are being tried, they do not register in the DNA of the type. Then they
might begin to find ways of accurately estimating when emergences occurred and how
long bifurcating lineages took to acquire their visible features. This is the difference
that emergentism makes to the whole conception of evolutionary rates.
What Difference Does Emergence Make to the Concepts of Adaptation and

Adaptive Radiation?
For selectionists, real evolution is adaptation under competitionuseful, genetically
determined variations are selected and become general features of populations.
Therefore, the question What is it for? drives their primary methodology, closely
followed by What was the selection pressure that popped it? I can demonstrate the
inadequacy of this approach from personal experience. Tom Fenchel and Rupert Riedl
conceived the thiobiosa trophic structure based on the energy of sulfurin 1970.
Shortly after they published, Fenchel explained to me that the benthic thiobios co-
existed with the primary productivity of photosynthesis in the water column above.
Since either kind of primary product was useable as the main food source of the clams
that I researched, I was mildly baffled at the significance of the thiobios. However, it
was illustrated dramatically when thiobiotic marine thermal vent communities were
discovered about a decade later. The point was driven home in my later studies of
lucinoid bivalves, whose symbiotic nature and place in the thiobios had just been
discovered. During that research, I came across several earlier authoritative answers to
the anatomical What is it for? question.6 Those ingenious adaptationist interpreta-
tions had nothing to do with the sulfur oxidation that is the primary source of energy
for these animals. Unfamiliarity with the symbiosis led to meaningless explanations
of anatomical variations in terms of their selective advantage. Yet because any selec-
tionistic conclusion was enough to terminate the search before the real answer had
been found, no one had questioned its deficiencies. It was valid within the paradigm,
but it did not represent any kind of intermediate step on the way to the truth; rather
it was an impediment to further progress.7
An emergentistic interpretation is radically different. The virtually all-or-none estab-
lishment of a sulfur-oxidizing symbiosis had multiple effects, including behavioral
change, digestive-tract regression, paedomorphosis, and structural alterations in gill
filaments that housed the symbionts. There was no selection pressure for any of
thesethere never actually is a selection pressure. The generative conditions were the
clams epigenetic and physiological adaptabilities, in the context of a high sulfide
412 Chapter 11
environment that was inclement for many other animals, but happened to be
inhabited at its fringes by sulfur-oxidizing bacteria. These then became symbionts
when larvae fed on them. Even at that stage, the symbiotic lucinoid clams persisted at
interfacial environments with access to reduced sulfur for nearly 200 million years,
without major diversification. That only occurred in the wake of K-T, the Cretaceous
termination event, when decomposing competitors spiked the soup with sulfide.
For most neo-Darwinists, adaptive radiation, or any kind of large-scale evolution, is
no more than slow, cumulative adaptational divergence. From the emergentists point
of view, the typological, essentialistic organism, long despised by Ernst Mayr and his
disciples, must make a comeback. The multifunctional emergent properties of an
archetype are what make specialization of divergent adaptive lines possible. Although
the directional exaggeration of simple adaptational features through selection are also
possible, a number of the component steps are allometric critical-point emergences,
and some may be saltations that occur despite selection.
Once the archetypes of the animal phyla were in place in the early Cambrian,
further saltatory epigenetic emergences produced the founding members of the classes
and lower taxa. These were not progressive in all cases. In mollusks, experiments in
shell form, combined with allometric shifts, exemplified by the huge expansion of the
posterior region of giant clams, could have been all that was necessary for diversifica-
tion. Paedomorphosis, which is common, is a regressive process. Regression of
segments and limbs was important in the diversification of Arthropoda, following
their initial repetitive differentiation. Class Crustacea has a great diversity of forms. In
comparison, a casual observer might think of insects as being all much of a muchness
in body plan, although diverse in habit. But primitive insects had to go through
various emergent stages. Reduction of the number of legs as a function of Hox gene
mutation has been demonstrated by experiments on the multi-limbed brine shrimp
Artemia.8 Somehow the six-legged condition became an archetypal feature of all future
insects. That sets us another problem. The number of legs in spiders is eight, and there
are ten in decapod crustaceans. An analogous case is that of the unsegmented
Cephalopoda: octopuses have eight tentacles; squid have ten. Are those numbers so
crucially adaptational that they occurred and were selected numerous times in each
group? Or did each group diversify from a few archetypal organisms that coinciden-
tally happened to have the characteristic number of limbs along with a constellation
of more meaningful qualities? In the case of the insects, a pair of antennae were also
characteristic of their multiple properties, but wings were not. Numerous when they
were first acquired, they were reduced to four and then to two.9 Later on, some
acquired holometabolic metamorphosisthe striking caterpillar to butterfly and
maggot to blowfly transformations. To achieve this, epigenetic innovations, especially
those that caused anatomical differentiations and heterochronous delays in the larvae,
were required.
It is easy to get lost in the evolution of form when discussing diversification. But
some of the most significant emergences among insects came with the acquisition of
symbionts, and the biochemistry and physiology that accompanied them. Wings are
a sine qua non for taking to the air. But certain physiological functions and behavior
are also crucial for flight, as well as for reverting to the water. As for the vertebrates, it
cannot be emphasized enough how a sophisticated homeostasis is the foundation of
their diversification, and how physiology, behavior, and development have boot-
strapped each others evolution. Nor is the environment simply a backdrop to be
adapted to. It has directly interacted with the internal milieu, imposed epigenetic
change, limited some behaviors, and afforded open access to others. And while all that
was going on, the environment was being geophysiologically changed by organisms.
Saltatory emergence and orthogenesis are too unruly for the Modern Synthesis,
which stands or falls by the premises that natural experiments are all small and
random, and that those that are adaptational are gradually accumulated by natural
selection. However, orthogenetic trendsin officialese, allometric shiftsare major
components of so-called adaptive radiation. They are also quite ruly by epigenetic
standards. Although the initiating experiment in replication slippage, gene
duplication, cell duplication, or cellular topography is probably random, it can
continue to amplify itself in its own lineage without involving selective advantage
in its incipient stages. If it finally becomes disintegrative, it does not need a metaphor-
ical force to supervise its extinction.
When orthogenetic trends reach a critical point of improved utility the emergent
potential can be magnifiedorganisms can change their behavior to let function
follow form. As easily as Slijpers little goat took to bipedalism, a reptile or a placental
mammal whose forelimbs had been epigenetically reduced could do the same. Then it
could choose to use forelimbs as hands, butterfly nets, stabilizers, gliding organs, and
ultimately wings. But it would stop using them to dig burrows or to break into termite
nests. Orthogenesis, as a motor of diversification, would displace natural selection to
the end of the allometric assembly line. Simple adaptations, genetic variants that
dominate in particular external or internal environments, are real phenomena. Their
accumulation cannot result in progressive evolution, instead they draw our attention
away from it.
Eventually, most experiments in emergent evolution were to fall into dynamic
stability, with the most efficient use of resources, specialization into new niches
partitions, and diminution of the potential for further change. This is what the
Darwinist image of the adaptive radiation wheel conveys. There is a hub, represented
by the ancestral type, and its divergent, specializing descendants radiate out gradually,
like spokes. It is a metaphor required by a system of thought based on the directional
and gradual accumulation of adaptations. Ad hoc hypotheses explained the absence of
intermediate forms: they were outcompeted by their descendants, and so rare as to
414 Chapter 11
escape fossilization. This is oversimplification, if not fabrication; most of the links are
missing because they never existed.
Because of these complications, the purest textbook explanations of adaptive
radiation are given at the genus level. Darwins finches are perennial exemplars of
evolution in action through purely adaptational diversification. But how pure is it;
how might the revision of natural selection and application of emergentism affect its
interpretation? Are the Galapagos finches the products of gradual selection of
insensible adaptational steps, or of saltatory emergence?
Their functional anatomy and behavior diversified relatively recently from that of a
South American seed-eating ancestor. The beak and associated head structure of these
finches are discontinuous, differential expressions of neural crest organizer cell action,
and bone morphological protein genes (q.v. chapter 5). However, convention ignores
the epigenetic origin of beak monstrosities to look instead at the one true cause
natural selectionespecially when the conditions of life change. This essentially
comes down to competition for food. If only small seeds are available, small-beaked
birds have the highest fitness. Also, the exclusion of large-beaked finches may addi-
tionally change the genetic environment so that the beak size may be affected, say by
increased homozygosity. Just how much speciation in the conventional sense has
occurred in the Galapagos genus Geospiza is debatable. Peter and Rosemary Grant,
those sterling observers of the Galapagos finch species, have found that their hybrids
are viable.10
John Gerhart and Marc Kirschner argue that developmental studies can help us to
understand the specific factors and interactions altered in the course of selection-
driven evolution.11 From what they immediately add, I can only understand such a
statement as another genuflection to selection by authors wary of assault by ultra-
Darwinists:
The rapid diversification of beaks suggests that any of a variety of mutational changes may be
enough to generate new morphologies and change size, perhaps reflecting the manifold
regulatory contingency of beak development. The emergence of successful or functional mor-
phologies in variants may not be a complete accident, but may reflect the kinds of hierarchies
and compartmentalization of developmental processes, ones that tend to produce functional or
at least nonlethal anatomies, rather than ones with serious mechanical defects. This shows up on
the robustness and flexibility of the processes. . . . In light of the networks characteristics, change
is probably not random.12
And yet it is selection-driven?

Besides the fecundity and brief generation time of Darwins finchesbirds born in
the spring can be grandparents by the fallthere are two possible reasons for rapid
demographic responses to environmental change. Beak epigenesis might still be more
loosely canalized than in the ancestral continental populations. But it may just be a
pre-existing polymorphism, some of the beak morphs normally occurring only in
small numbers at the fringes, or recessively lurking out of sight.
From the emergentists point of view, the finches that were rafted or blown to the
Galapagos from South America entered a pristine environment almost devoid of avian
competition, but which immediately called into action remarkable physiological and
behavioral adaptabilities that the birds already possessed, prior to adaptational adjustment.
Clios African grey parrot Mungoa seed eater, and very fond of sunflower seeds and
pistachiosis intrigued by the taste of snails, and the crunchiness of their shells, but
does not care to have his beak gummed up with mucus. However, he will ingest and
digest mangoes, ice cream, earthworms, wireworms, chicken wings, prawns, crab legs
(shell on), barbecued steak, and parts of visiting primates that get within his reach. His
behavioral repertoire goes beyond mimicking sounds, to associating words with
objects, reading body language, and cajoling us to communicate, entertain, and preen
him.13 But his wild conspecifics are constrained by competition and predation to be
less versatile. This might underrate parrot cognition. Clio has also done some field
research on the New Zealand alpine kea parrot under the direction of Ludwig Huber.
She remarks that wild kea are not neophobic, i.e., scared away by strange things. They
show great interest in human activity and can be induced to explore human artifacts.
But they also exercise their option of becoming bored and flying away, rather than
sticking around and responding to the more complex experiments that are possible
with captive birds.
In some regards birds are more adaptable than humans. A television documentary
was made about the death zone above 6,000 meters on Everest, where so many
climbers have died, even when equipped with supplementary oxygen. It failed to
remark on the Himalayan crows that flew overhead, wondering what all the fuss was
about. G. Ledyard Stebbinss comment that the ability of the bar-headed goose to fly
high in the Himalayas was due to the selection of a mutated gene for hemoglobin was
unmindful that it was a small part of the emergent constellation of birdness, because
that, of course, would be essentialism.14 And there are the Arctic cormorants whose
adaptability allows them to regress to an apparently non-adaptive conditionto
diminish their thermoregulatory ability under conditions of extreme cold stressand
yet thrive.
Darwins finches are birds; not disembodied beaks, far less genes for beaks. When
they first arrived in the Galapagos, their avian adaptabilities enabled them to deal with
dry or wet, hot or cold conditions, to eat and digest seeds, fruit, insects, or snails.
Founder effect and hormonal destabilization may have strongly influenced epigenetic
homeorhesis in the small population of invaders, restoring a primitive plasticity to
beak formation until populations filled out and selection took charge, putting a
premium on birds with beaks that could keep up with the competition. They could
experiment further with functional morphology, complemented by behavioral and
physiological adaptability, given more freedom from natural selection. But selection-
ism is forced into ad hoc adaptational speculation. In contrast to conventional
416 Chapter 11
adaptive radiation, Darwins finches illustrate the constraining effects of competition,

and the speed at which adaptability and diversifying experimentation can act in its
absence.
I once looked after a baby robin whose exploratory bent had taken far enough for
its nest to be unfindable. After a day, and much gulping of worms from a pair of
forceps, it imprinted on me, flopping along as fast as it could to stay located between
my feet. Every time I glanced down to avoid stepping on it, it looked up at a 6-foot,
200-pound colossus and gaped for more food. This hopeful little monster would not
have lasted another hour in the wild, under the scrutiny of ravens and bald eagles. But
given protection from the slings and arrows of natural selection it might have started
a new lineage of robin pioneers, ready to take full advantage of their essential birdness.
Another example of adaptive radiation is an even better trial of the Darwinist rule.
The cichlid fish can evolve at a dizzying pacehundreds of species live within just
three African lakes, and many of them seem to have emerged overnight. This is a
1999 Scientific American editorial comment regarding an article by Melanie Stiassny
and Axel Meyer, Cichlids of the Rift Lakes.15 Overnight is not an exaggeration in
a Darwinist time frame, since much of the speciation in Lake Victoria occurred after it
dried out and then begin to refill 14,000 years ago.16 The windows of opportunity got
narrower in Lake Nabugabo, which was isolated 4,000 years ago, and has five endemic
species, and at the South end of Lake Malawi that was dry two centuries ago, but now
has numerous species and color morphs that are found nowhere else.17
By this time you should not be surprised, since you know that by our interpretation
of emergent evolution any organism invading a pristine environment can diversify as
fast as its isolation, the resources, its behavior, its physiology, and epigenetic and
genetic accommodation will allow. And we have already been talking in terms of
months and years, not geological epochs. This argument is complemented by
Stiassnys and Meyers own explanation of the generative conditions of the cichlids
evolutionary diversification. First they point to the provision of isolated environments
because of climatic changes. Next comes the adaptability of the double jaw structure,
which can be put to use for eating plants, grazing on encrusting algae, picking off
insects, mollusks, ingesting sand and sorting out edible infauna. The cichlids may eat
zooplankton and the eggs, young, and adults of other fish, and they may even nip off
the scales of other cichlids.18 The inner jaws evolved in the same way as, but later than,
the outer mandibles of all gnathostome fishby exaptation of gill arches. Although
the feeding behavior is usually species specific, the double jaws remain epigenetically
malleable: They can change form even within the lifetime of a single animal. (Even
the teeth might transform, so that sharp, pointed piercers become flat, molarlike
crushers.) Cichlids that are fed one kind of diet rather than another can turn out to
look very different.19 Loose canalization of development has allowed the parallel
evolution of five behavioral and morphological specialists in Lake Tanganyika and
Lake Malawi. Another condition for emergent diversification is an unusual degree of

parental care. Many cichlids protect their eggs and young in their mouths, where they
can also share scraps of food. This parental care allows persistence of the species
despite relatively small numbers of offspring and small populations.
Where Does Speciation Fit In?
The diversification of Darwins finches and African cichlids brings us right to the
speciation problem. We can deal immediately with one evolutionary aspect of
speciation, without serious objection from any faction. It pins the ratchet of evolu-
tionary change by diminishing the loss of phenotypic, organismal uniqueness
through sexual reproduction. Imagine a world without biological species, where all
types could interbreedwhere pollen in the air could produce miscegenies as well as
allergies. The speciation curb on natural experimentation reduces the generation of
ragweed babiesgimcrack hybrids that would fail the integrity test. There is a tradeoff
between evolvability and speciation, just as there is between evolvability and the
phenotypic integrity of the organism. To refer, as I have, to species as a mental
construct is not entirely dismissiveall our theories and concepts are mental
constructs whose survivability is independent of nature. To me the biological species
concept, based on the reproductive viability of the members of populations, comes
close to a satisfactory pragmatic definition, if such a definition is required to justify
the continued use of species as a universal taxonomic unit. Even so, it has fuzzy
edges wherein lie recognition, and accessibility factors.20 My real objection was to
the Darwinian notion of speciation by accumulated adaptations, which is a different
can of (perfectly adapted) worms.
Linnaean systematics had few evolutionary connotations, and so engendered little
dispute, while making the immense diversity of living organisms seem more
manageable. Classification into species brings order into confusing diversity, which
was attractive to Enlightenment philosophers. Furthermore, the giving of names and
the naming of names has always had mythic proportions for humans. Even in science
there are metaphysical implications of possession and control by namers and definers.
So the psychological impact of the species concept was already strong before Darwin
came along. Therefore, Darwins explanation of the origin of such real categories must
have been highly alluring or provocative, according to the mindsets of his individual
readers. One way or another, they were all excited, which helped to mask the fact that
Darwin actually had little to say about how species originated, and a lot to say about
what happened afterwards.
The conventional wisdom of The Origin of Species proposed that once new species
had arisen through the adaptational diversification of a founding group then the
major evolutionary rite of passage had been satisfied. Speciation events are still
418 Chapter 11
portentous, even for biologists who doubt the primacy of adaptation. Could it be that
they are putting the cart before the horse; that they are instead referring to emergence
events or simply environmental events that are then followed by speciation? That
being the case, speciation could be epiphenomenal to emergent evolution and drastic
environmental changes, rather than a causal process. This is not to say that epiphe-
nomena are insignificant. For example, mind is an emergence, and is also an
epiphenomenon of brain structure and function. And the causal impact of mind takes
it far from being a mere babble of a brook. Nor should we rule out adaptational diver-
sification as a process that hastens speciation. Yet speciation could also occur in the
absence of emergent or adaptational evolution, as a consequence of isolation and
genetic drift. To evaluate these alternatives, it helps to know how and when speciation
has occurred. Most of the species with which we are presently familiar, through
observation of generations of living representatives, or through the fossil record, or
both, as in the example of Homo sapiens, are remarkably fixed. For selectionists,
however, it is evolution when cryptic characteristics appear phenotypically under
unusual environmental change, or simply when the numerical distribution of alleles
is altered. To the contrary, the species as a whole may still actually be in stasis.
Regardless of which stage of cladogenesis an organism has reachedthe final
bifurcation of a genus, or the primary bifurcation of a classit belongs to what we
would pragmatically call a species. But the former might be doomed to stay where it
is, while the latter could be the archetype of the whole class, perhaps because it was in
the right place at the right time, or because an apomorphic or key emergent feature
gave it a specialized function, or an unusual adaptability, or because it was in an
unusually loose state of primitive epigenetic canalization.
In summary, speciation may occur in the wake of various events that provide some
kind of isolation. These include any emergence that makes members of the old
population unavailable for breeding and results in sympatric speciation. Second, it
may come after catastrophic change in the environment that disequilibrates the old
dynamic stability. Third, it may follow from the invasion of a new environment, with
organismal relocation (usually referred to as gene flow in the literature of population
genetics) obstructed somehow; i.e., standard allopatric speciation. These ideas are to
be found in any textbook. But their conventional interpretation leaves the impression
that speciation is an evolutionary cause rather than an effect, and would reject the
notion that speciation is epiphenomenal. Random changes in isolated populations
that culminate in biological speciation need not amount to significant evolutionary
changein contrast with evolution defined as changes in the distribution of alleles in
populations. The event needs to be logically separated from the speciation.
Another aspect of speciation that might be affected by an emergence synthesis takes
us back through the Looking Glass to species as units of selection. These are the hierar-
chical levels at which natural selection is purported to act. In ascending order they
include genes, epigenetic cell lines (or creodes), organs, organisms, groups, species and
ecosystems. Darwin sensibly settled for selection at the organism level, though his
position was made uncomfortable by sexual selection, which seemed to go in the
opposite direction to natural selection. Still, sexual choices happened in nature, so
they must be natural too, though eliminated if they went too far astray. I have argued
that selection is a consequence of emergence, but does emergentism see any real
biological phenomena that are reflected in the mirror as selection of this or that unit?
Where, as the selectionist might say, is adaptiveness manifested?
Below the organism level, it is conceivable that any gene mutation, cellular differ-
entiation, or organ exaptation might result in an improvement in survivalother
things being equal at all the other levels. The only arguments that I would give selec-
tionists on this point are, first, that all other things are never equal; there are
epigenetic and homeostatic adjustments, and other differentially advantageous events
that have to be considered in the organism as a whole. Second, such improvements
might be dramatically sudden, rather than through slow adaptational accumulation.
In any case, it is above the organism level that the Looking Glass war of selection units
is waged.
To keep the smoke in the mirror to a minimum, we might start by extending
Darwins view of sexual selection. Now, although Darwin usually concentrated on the
fitness of the individual organism, here the interaction of a mating couple came into
the picture. And the selective choices were real. The sexual synergy of the pair makes
it a whole that is greater than the sum of its partsespecially one that successfully
produces offspring.
The concept of a whole can be extended beyond reproductive interactions to groups
that cooperate in defense, shelter, and nutrition as well. Conceptually we might be
dealing with anything from biofilms made up of various unicellular organisms to
insect societies or human social groups. Removal of an individual from such a whole
might have a negative effect, as might rearranging the dispersal or behavior of
individuals within the group. Thus, William Wimsatts definition and test of an
emergent whole, in contrast to an aggregate, applies to such groups; q.v. chapter 7 of
the present volume and Wimsatt (1997) on aggregativity. Remember that we are
looking at the whole from the point of view of its proximate emergent properties,
rather than its ultimate differential reproduction. To view the group in isolation in
this way is still too restrictive, because there is interaction between it and the groups
of other species in the community as well, not just as competitors, or predators or
prey, but sometimes cooperatively or symbiotically. The emergent properties of the
group, or the ecosystem for that matter, make it not just a unit, but a whole that is
greater than the sum of its organisms. Moreover, it might expand, or, more likely,
extend satellites of itself into new environments, where it might take over from the
groups already in occupation of them. This is more a matter of ecological succession
than evolution, yet it crudely recapitulates evolutionary history.
420 Chapter 11
To say that groups have holistic qualities is as far as it need be taken. It is

unnecessary to venture through the Looking Glass, to insist that such groups are
selected, or that they were created by natural selection in the first place. It is even less
profitable to gaze through the glass darkly to where species are selected, because
species, and for the most part populations, are not emergent wholes but aggregates. In
a recent personal communication, Michael Ghiselin, whose idea of the species as an
individual inspired the popularity of species selection, says that species do all sorts
of things that organisms do not. For instance, they speciate. That puts any species in
the ranks of emergent wholes. However, it is one thing to invent an inspirational
analogy, and another to give it material reality by fiat. If we could escape the
population-thinking bind of the mid twentieth century, we might see that species
cannot speciate. Only individual organisms and some of their close relatives speciate.
Those can be selected in the conventional sense because they are integrated wholes.
But the rest of the species members get left behind. Unless a species is so few in
number that all its members interact, it is not a whole but an aggregate. Therefore,
species have nothing selectable that is not found in their parts, i.e. the individual
organisms. Indeed, to put it more provocatively, species may simply be reifications (i.e.,
Theres this big important word species, so it must represent something real). To
take away, or rearrange the individual members of a species might have no holistic
impact whatsoever, until those changes reduced the totality of the species to a group
or groups whose emergent properties would then be affected by further attrition. For
these reasons, I am inclined to accept V. C. Wynne-Edwardss discredited 1962 concept
of group selection and to dismiss the currently popular species selection.
What Difference Doesnt It Make?

In the absence of appropriate theories or syntheses, life goes on, and so does biology.
Most of the work that I have cited in this book was done by people who would auto-
matically call themselves Darwinists or neo-Darwinists. Good biology is done by
people who are fascinated by living organisms, their internal interactions, and their
environment, regardless of the kind of theory that they superimpose upon them. If
you look at the outstanding general textbooks on introductory biology that are
presently on the market, you will read chapter after chapter, dishing out good biology
without reference to natural selection, although the Find-The-Selection-Pressure game
is becoming more intrusive. Good biology is even done by people who start from
ultra-Darwinist theory and attempt to confirm, verify, or nullify it. Everything that is
seen within the Looking Glass obeys the physical rules of action and reactionand
optics. It makes sense, even in mirror image. Studies of adaptations and selective
advantage reflect the qualities of emergences under particular circumstances; so they
are an indirect path to reality. But would life not be simpler, and logically more
sufficient, if all those good biologists went directly to the crux of evolutionary change?
That gives us part of a response to the next awkward question.
Does It Even Matter?

In a 1988 essay, Marjorie Grene asks Is evolution at a crossroads? and concludes that
the New Biologists and complexity theorists present a significant challenge to
orthodoxy. However, considering the history of the Darwinian tradition, the
challenges it has overcome and assimilated in the past, I would predict that in this case
again it is probably a Kauffmanlike expansion rather than a Goodwinlike replacement
that will occur.21
In my opinion, recent expansions (or shifts of evidence) have pushed the envelope
of the Modern Synthesis to its limits, demonstrating that replacement is the only real
alternative (West-Eberhard 2003; Kirschner and Gerhart 2005). We are stuck with a
synthesis that has perennially resisted any kind of revolution, or assault, or even sober
Baconian diplomacy. It has instead absorbed and expanded and forgotten where it has
been, until the next lot of sea lawyers rise in the mess to tell it where it is now, and
where it ought to be going, which is nowhere. And it is not easy to say so without the
irritated tone of voice that Grene and West-Eberhard dislike, because the success of
the Darwinian tradition has not depended on logic or evidence, but on sophistry,
polemic, authoritarianism, me-tooism, and, worst of all, indifference. For many evo-
lutionists, the statement if it exists it must have been selected [because it must
therefore be adaptive] is a truism that makes anything to the contrary seem
irrelevant.
In attempting a theory of emergent evolution, and its synthesis with a re-invented
natural selection, I have no claim to originality or priority. Nor does dissidence of itself
generate good alternatives. But ever since The Origin of Species was published, those of
us suspicious of selectionist explanations of evolution have looked to the more
fundamental causes of biological novelty. Independently we have drifted into the
three-ring circus, finding ourselves surrounded by empty seats and the ghosts of
Mivart, Cope, Bateson, Schmalhausen, Goldschmidt, Croizat, and company. We know
its the right place to be once we have seen what performances can be mounted, after
the conservative ringmaster, natural selection, has been sent off.
The idea that natural experimentation is what you put in its place was initially a glib
response to divert attention away from the causal role of natural selection, en route to
finding the intrinsic origins of evolutionary novelty. It left natural selection a comple-
mentary role of consolidating successful emergences by contributing to the
re-establishment of physiological and ecological equilibria. What is selected is
emergent quality, and it is the evolution of that quality that poses the major question.
Natural experimentation generates other metaphors, some pertaining to laboratory
experiments in molecular biology. It operates randomly within the constraints of its
generative level, like scientists who have just developed a new technique saying Lets
try it this way now, and see what happens. But out of random experiments there
emerge self-generating processes that continue along particular lines of research.
422 Chapter 11
Already in general use, the metaphor of natural experimentation is particularly

relevant to epigenetics. Hopeful monsters are natural experiments. What kinds of
conditions make them successful, and how complicated can such experiments be?
They involve whole organisms in complex environments, not simply mutant genes,
whether they arise randomly or under direction from the environment. We have
plenty of evidence from nature and from the laboratory to show how heritable char-
acteristics can be acquired by transgenesis, and how radical changes can be induced in
epigenesis. How many more of our laboratory experiments might have been tried
naturally during evolutionary history?
A final response to What do you put in its place? must deal with the metaphysi-
cal gap that would be left by the removal of natural selection from popular
consciousness. This brings us back full circle to adaptiveness, a usage I have tried to
avoid because it conflates adaptability and adaptation, and is in lockstep with natural
selection. Adaptiveness, if it must be retained as a biological term, should have the
primary sense of contribution to the persistence of organismal wholeness, which is
often self-sufficiently independent of external conditions.
Postmodernism wants to leave the wreck of the Modern Synthesis as an
Ozymandian memorial to paradigmatic obtuseness. I cant be too critical of the
movement since I myself am skeptical of institutionalized ideas. But I have a mission
to launch a theory of emergent evolution, and try for a biological synthesis, rather
than to bob around with the motley flotilla that presents the postmodern
smorgasbord. I dont want to go beyond reductionism with Koestler and Smythies
(1969), beyond neo-Darwinism with Ho and Saunders (1984), or beyond natural
selection with Wesson (1991). I want reductionism and neo-Darwinism and natural
selection to be seen for what they actually are, and then find a different synthesis. Such
a synthesis would be interdisciplinary as well as dialectical, since it must involve more
than the conciliation of a set of apparent contradictions. Post-Lamarckism, structural-
ism, complexity theory, the lucky-strike paradigm of neo-catastrophism, evo-devo,
and symbiosis studies all focus on important elements of evolutionary causation. But
their individual adherents, whether modern mutineers or postmodern privateers, lack
the resolve to escape the vortex of Darwinism. If they do not all hang together in a
new synthesis they will all hang separately, to be scavenged by the Modern Synthesis,
stuck in the hold, and forgotten. That seems to have been the fate of the New
Biology of the 1970s. Although it tried to change the paradigm, it needed more than
groupthink enthusiasm to hold it together.
From the outset I have shown that the most important emergences involve
progressive improvements in the general features of biological self-organization, and
physiological and behavioral adaptability. In the case of plantslest my zoocentrism
makes me forgetthe emphasis has been on reproductive adaptability, bootstrapped
by the evolution of animal pollinators. These progressive evolutionary changes hang
on through self-sufficiency, without high fitness, during the prevailing times of

dynamic stability. In other words they persist regardless of natural selection qua differ-
ential reproduction.
Emergentism does not contradict the perception that most dynamic structures in
their development and actions are correlated with the persistence of the organism in
its own being and the persistence of its descendants in future generations. In that
sense it does not contradict the role attributed to natural selection in popular con-
sciousness, and it accepts that the metaphor of selection pressure has been an
inductive guide on occasion. However, it rejects outright the reification of metaphor
as a creative force, whether it be selection pressure or Lamarcks organism-responding-
to-a-need.
The re-invention of natural selection should be enough to shiver the timbers of the
Modern Synthesis, and confront ultra-Darwinistic extrapolations that have already
infected anthropology, psychology, economics, and philosophy. Since the universe
never unfolds the way it ought, selectionists, faced with such a prospect, are more
likely to go into a state of denial, or to shoot the messenger. The spectators hate to be
told that the Emperor is naked, because they knew it all along, and it is less humbling
to continue the mass pretence than to come out and admit self-delusion. But beyond
whistle blowing, emergentism proffers a holistic emphasis on the importance and con-
nectedness of every aspect of life. For this a metaphysical yearning existed long before
Darwin, and far beyond biology. Deeming it irrelevant, analytical selection theory has
failed to satisfy that need.
As a minor effect the constant adduction of natural selection to any evolution-
ary insight would no longer be necessary, and this drain on freedom of thought would
cease. Casting around for the explanation of any biological phenomenon in terms
of gradual accumulations, subtle correlations of insensible advantages, and arcane
selection pressures would be unnecessary. The weak knees of dissenters would
enjoy relief from genuflection to the hypostasis of natural selection. The significance
of adaptiveness would not be diminished, but would not be a Looking Glass reflection
of emergent quality. As adaptability, it would be seen in the context of complex-
ification of the essentials of life, and as adaptation it would remain a relative feature
that contributes to stable equilibria, whether physiological, developmental, or
environmental.
The larger problem for biology is simplistic reductionism, to which ultra-Darwinism
is naturally allied. The solution lies with realistic holism, also known as interaction-
ism, the natural ally of emergentism. Nevertheless reduction would remain paramount
in some thought experiments, and in the laboratory, where molecular biology would
continue to demonstrate mechanisms that participate in emergence. The reductive
and synthetic consilience that E. O. Wilson calls for is necessary, but not in a form
where reductionism leads as the way and the light.
424 Chapter 11
Realistic holism need not lead to an unfocused research program that tries to do
everything at once. Particularized research would continue as usual. A comprehensive
comparative biology with an emergentistic outlook would be a check on the hubris of
specialists who believe that their topic is the most important in the business. No single
discipline has a lock on the hidden treasures of evolution. Particular research results
need to be cross-referred to other programs, so that nobody is out of the loop.
Holistic evolutionary studies should discover the lateral relationships between
traditional disciplinesthe three ring circus of epigenetics/form, physiology/
behavior/function, symbiosis/society under the big top of an ecology that does not
forever strain to abstract the environment to numbers. Within them there are hierar-
chical relationshipsfunctional morphology relates up to behavior and down to
biological molecules. Intolerant reductionism has no place in an emergence program;
nor does a hylozoism that forces the characteristics of higher emergent levels onto
lower ones. New rules emerge at each new level of progressive evolution, and their
identification requires knowledge of the organism and its relationships. These
common sense guidelines are already followed by a good many biologists, but at a
time when organismal biology is nearing extinction they need to be loudly
proclaimed.
The significance of founder effect would be elevated, since innovation finds its best
expression among a small number of organisms with closely related genetic and
epigenetic combinations that are not overwhelmed by a disapproving crowd of old
family relatives. Speciation is already being played down as a central issue of evolu-
tionary theory within the Modern Synthesis, so emergentism would only
re-emphasize that the origin of species is not the pivotal process of evolution. Cladistic
systematics, which concentrate on emergent characteristics of bifurcations, would be
supported and extended, since emergentism emphasizes a comprehensive understand-
ing of generative conditions and the full constellation of emergent properties.
However, some distinctive apomorphic features of a clade-founding type may have no
adaptive meaning. Gout is not characteristic of Dalmatians because it has some cryptic
adaptiveness for spotted firehouse dogs, but because the few original sports were
careless with the genes for nitrogen metabolism; and the same may be true for gout in
the hominid lineage. At a given focal generative level there is insufficient time and dis-
crimination for internal relationships to be fine-tuned to perfection before it takes off
again to a new emergent level.
Emergentism would give different direction to research. The greatest unknowns
were in epigenetics and developmental evolution. The Modern Synthesis has tradi-
tionally been hostile to these because of their saltatory implications. Evo-devos are
increasing in number. Old hypotheses based on physicochemical morphogenetic
fields are being revived. Once an almost perennial theme of evolutionary embryology,
they had been discarded by the genocentric phase of the Modern Synthesis. The
widespread phenotypic consequences of early changes in cell lineages are being

analyzed. And the significance of the deep homology of homeotic gene groupings that
universally organize limb and eye structures has become so widely recognized that one
neo-Darwinist calls them clich storiesin other words, tiresomely awkward for
the conventional explanation, so please stop going on about them.22
We would be in a better position to make predictions if the accommodatory
mechanisms for radical epigenetic evolution were fully understood. The human
genome project is spinning off information relevant to the role of viral transduction,
especially of bacterial genes, and its other discoveries might be taken further with an
emergentistic rather than a selectionistic impetus. And the same goes for the
evaluation of epigenetic drives in allometry or orthogenesis, if they are allowed to
come in from the cold. There is no shortage of causes to be investigated in the light of
emergentism. One outstanding but relatively unexamined database is in agriculture.
And where better to start than Darwins 1868 workbook The Variation of Plants and
Animals under Domestication? Though all of them might be recognized as legitimate by
conventional evolutionism, they still need to be integrated into a single synthesis for
which emergentism offers a framework.
Who Cares?
After about 70 years of neo-Darwinism and ultra-Darwinism, there are more than a few
biologists and philosophers who see the limitations of selection theory, and some
who, like me, reject it altogether as a significant evolutionary cause. Throughout this
book I have alluded to the others I find significant. Eugene Balon (2004) provides
further insight into the paradigmatic crisis that I mention in my introduction.
Irritated voices abound. A final broadside at the ultras would be out of place here.
However, there is one case history that I find striking.
The biological historian William Provine is the author of The Origins of Theoretical
Population Biology (1971), a book that I found most helpful while writing my 1985
book Evolutionary Theory: The Unfinished Synthesis. Provine attributes the strength of
neo-Darwinism to the popular appeal of P. M. Sheppard and Theodosius Dobzhansky.
The influence and success of Richard Dawkins and Stephen Jay Gould would seem to
bear Provine out.
In his 1988 essay Progress in evolution and meaning in life, Provine eventually
came round to the opinion that the Modern Synthesis in America had been a constric-
tion of evolutionary theory, more characterized by what it rejected than what it
included. Interestingly, his afterword to the 2001 reissue of The Origins of Theoretical
Population Genetics indicates that Provine has become more impatient with the wait.
He now believes that natural selection has no causal role in evolution. Furthermore,
he manages to avoid the irritated tone of voice:
426 Chapter 11
In 1970 I could see the origins of theoretical population genetics as being an unalloyed good for
evolutionary biology, and thus obviously a great subject for a historian. Now I see these same
theoretical models of the early 1930s, still widely used today, as an impediment to understand-
ing evolutionary biology, and their amazing persistence in textbooks and classrooms as a great
topic for other historians.23
Welcome to the circus.

I suspect that many conventional biologists have the subconscious feeling that the
current paradigm is bolstered by too many ad hoc hypotheses, and that the trend to
ultra-Darwinism is puritanical rather than rational. Darwinist cant about fitness has
already extended as excellence in everything from sport to education: the winner
excels over all the rest, who therefore do not count, except as an admiring audience.
Emergentism looks out for the rest, especially those who avoid the competition.
Liberation from these burdens should be inspirational in itself.
The Cosmological Foundation

What difference does it really make to big stuff such as cosmology and the origin of
life? This question plunges deeply into the metaphysics of emergentism. Asteroid and
comet strikes are small potatoes in this context, although the one that created the
moon about 4 billion years ago is hard to ignore since it probably extinguished any
life that might have existed by that time. It gave our planet tides that were initially
devastating to microorganisms with terrestrial ambitions, and leached the rocks at a
faster pace than at present. And tides continue to make the water/land interface
interesting. That vast primeval collision also affected planetary rotation and tilt, with
climatic consequences that make Earth more hospitable to adaptable emergents. But
these factors pale by comparison with the origin of the Universe. The appearance of
non-biological cosmological novelties fits my general definition of emergence as a
spontaneous innovation arising from the interaction of generative conditions. Calling
the cosmological Big Bang an enormous emergence points to its instantaneous
nature, and the subsequent complexification of matter with literal constellations of
emergent properties. Cosmologists have a major problem regarding the initial,
generative conditions, since they lay outside this universe. They were nonetheless
critical if the resulting universe was to have the inherent property of producing and
supporting organisms.
It is easy to talk loosely about the evolution of the chemical elements, stars,
planets, and pre-biotic chemical compounds. Given its unique initial (generative)
conditions, such complexifications over the course of time seem to have been
inherent in the Big Bangnot just probable, but somewhere and sometime inevitable
under the right physical forces. Timing and location remain, however, unpredictable.
In such a universe, with the passage of time, chaos must fall into an ordered
complexity of attractors consisting of galaxies, stars, planets, elements, chemical
compounds, and organic molecules that constitute the generative conditions of the
emergence of life. But this evolution, though it has emergent properties, has the old-
fashioned sense of an unfolding of pre-existent characteristics, unlike biological
evolution, which is reproductive and progressive.
This was the position taken by the psychologist William McDougall in his critique
of emergentism, Modern Materialism and Emergent Evolution (1929). He admitted that
the formation of a water molecule and a biological emergence were analogous. There
was a synthesis; the whole was greater than the sum of its parts, its properties could
not be predicted from an intimate knowledge of oxygen and hydrogen. But he saw
that the ability to form water was inherent in its elements; the synthesis was bound
to occur under particular physical conditions, and only in a narrow temperature range
would the fluid phase show its anomalies. Although the forms of crystalline water
varied considerably, they were obedient to local physical conditions. Once such a
phase shift had occurred it could regress to a more chaotic state, but a new emergent
level could not build upon the structure of ice. Biological emergent evolution needs
reproduction, which transcends chemistry, solid-state physics and quantum
mechanics. Only living organisms can reproduce their qualities, and project their
histories into the future. Only they evince the self-maintenance and adaptability that
can differentiate, specialize, and become more complex in ways that further enhanced
those fundamental properties. Even so, it is not quite that clean cut. There are inter-
mediate areas of physiology and epigenetics where external physicochemical
influences can persist for millennia without effecting reproducible gene changes.
Although I have given an accurate account of McDougalls distinction between
physicochemical and biological emergences, Modern Materialism and Emergent
Evolution was a critique of the curates egg style of emergence concepts found in the
writings of Alexander, Morgan, Strong, Noble, Broad, Sellars, Wheeler, and Jennings.
(A visiting curate was served a rotten egg for breakfast. When the Bishop asked him
How is your egg? he diplomatically replied Parts of it are excellent.) The word
McDougall used for heredity was memory. By equating the two he was attempting
to bolster his argument that biological evolution was purposeful, under the influence
of memory and mind. He was thus imposing a hylozoic point of view on all of life.
Hylozoism makes for some strange bedfellows. McDougall also believed in the
inheritance of acquired characteristics, on the basis of his own observations.
It is tempting to go along with McDougall part of the way and leave it there. But is
the qualitative barrier between non-life and life real, or is it illusory? Was the
evolution of our cosmos bound to generate conditions for the emergence of life, with
all of those novel properties? If so, the next phase of progressive complexification of
its offspring would be inevitable, and mind must finally emerge, despite obstacles
placed in its way by natural selection, and because of catastrophic events so disastrous
as to almost wipe out any progress that had already been made. Therefore, Stuart
428 Chapter 11
Kauffman would be right in saying that we are at home in the Universe instead of
leading a lonely, unique existence arising from almost impossible coincidences.
Emergent evolution is about the erratic journey from the origin of life to mind. We
can post-predict the conditions through which evolutionary progress was made, and
say that terrestrial bipedal homeotherms are probably the best candidates for the final
passage, but there are no inevitabilities about what lineage would have made it, or
where, or when, or how.
Paul Davies makes a useful metaphysical argument in The Fifth Miracle (1999). He
says we have to choose between two alternatives. One is a universe where the origin
of life is so improbable as to be almost miraculous, where, as Stephen Jay Gould said,
the tape of biological history could never be replayed the same way twice. The other
alternative is a panpsychic, deterministic universe, where mind is inherent in the Big
Bang, and must inevitably be manifested. However, in an emergent universe there is a
third, intermediate course of events. In the wake of the Big Bang, mass and energy are
likely to become heterogeneously distributed. Some locations predictably produce
carbon, oxygen, hydrogen, nitrogen, etc. Then there are rarer but still predictable
gravity wells where they will all accumulate, tend to stay together, and interact. There,
the potential for the origin of life might be high, though astronomically improbable
in the rest of the universe. The evidence keeps pointing to an early emergence of life
on Earth, almost as soon as it cooled sufficiently for liquid water to form. When life
emerged, it had no pre-determined role to act out. It did, however, have the ability to
act, and the ability to maintain itself, to reproduce, and to become more complex. We
might see prokaryotes as helpless victims of powerful physicochemical forces. But in
their microenvironments they do not behave entirely at random. This increases the
likelihood that they will be raised, through intrinsic and extrinsic influences, at some
place and time, to a new level of self-organization, to a new relatedness, which has
new rules of performance that do not contradict, but may supersede the old rules.
Thus, mind, as a manifestation of those novel internal relationships, becomes a likely
outcome at the higher levels. But it is not predetermined by the early generative
conditions. And it certainly does not reside hylozoically in the Big Bang nor in the
simplicities of solid-state physics.
Eric Chaisson might take a different stance. He is a natural successor of Alfred Lotka,
the thermodynamicist who noted that evolution is related to the increase in the flux
of energy through the biosphere.24 Chaissons survey of the expansion of energy rate
density as a function of increasing complexity in the Universe is set out in Cosmic
Evolution: The Rise of Complexity in Nature (2001). According to Chaisson, evolution,
sensu lato, is driven by energy flow. It then follows that the ultimate source of order
and complexity is cosmic expansion. In other words, biological evolution is not a
cause, but an effect. This conclusion, he writes, is sure to dismay most biologists.25
Well, he sure got that right; when I first encountered the argument, I felt hoist with
my own petardbut not for long. Somebody elses parallel analysis puts it this way:
For want of a nail, a shoe is lost. For want of a shoe, a horse is lost. For want of a
horse, a rider is lost. For want of a rider, a battle is lost. For want of a battle a kingdom
is lost.26 So horseshoe nails, or the lack thereof, are the causes of political revolution?
Give me a break! At consequent emergent levels there are spare nails, farriers, fresh
horses, reinforcements, smart generals, and the hearts and minds of the people. An
expanding universe has the potential to develop carbon etc. Carbon etc. have the
potential to originate life. Life has the potential to complexify through reproduction
now theres something the expanding universe didnt have in its hylozoic mindand
it is as a result of biological evolution that energy flow increases in the biosphere.
Cosmological emergences take on a different significance in the context of ideas
proposed by Andrei Linde, and extended by Lee Smolin in The Life of The Cosmos
(1996).27 Their fundamental principle is that in a meta-universal dimension, universes
generate other universes that all may have slightly different characteristics, depending
on their initial conditions. This excites one commentator to say the following:
Then even if most universes originally were tiny and very short-lived, natural selection, the key
Darwinian process, is bound to occur. Selection for what? For universes that are bigger and
longer-lasting, since those will produce the most black holes and effectively out-breed the
others.28
By this thesis, the type of universe most likely selected is one that generates stars that
generate black holes that generate new universes of a kind likely to contain carbon
and the potential for the origin and evolution of organisms.
Now, not-so-gentle but rather case-hardened reader, if you have actually read the
book in your hand instead of just picking it up to skim the last chapter, you should
know what to make of all this, cosmological mysteries notwithstanding. But let us take
it one last time, assuming that it is reasonable to apply the term emergence to
cosmology. Emergences are sudden and spontaneous, whether saltatory or of the
critical-point type. Their properties depend upon the combinatorial complexities of
the generative levelmatter/energy, gravity and whatever other ineffable forces might
be involved in cosmic emergences. If the emergent organism/universe has the wrong
total mass, or rapidly implodes, it dies without issue, and no additional agency is
relevant. If it is able to reproduce, it will do so without depending on any other causal
agency, and its offspring will reproduce according to their fecundity and the availabil-
ity of matter/energy.
Even by conventional standards of argument, natural selection only comes in where
there is competition that effects differential reproduction. In the cosmic meta-universe,
as well as under biotic conditions, space and resources have to be finite for
competition to make a difference. A novel organism in the absence of competition is
free to survive and reproduce according to its emergent properties. There is room for
430 Chapter 11
natural selection only where there is no room for all offspring to survive and
reproduce. That universes with carbon-based life forms are most likely to produce
similar offspring comes from their original emergent nature, not from natural
selection.
As a closed system (except that it might be spewing mass into the meta-universe
through its black holes), a universe is subject to no competition. If it has offspring,
their energy and matter are generated by the nature of the black holes from which
they emerge, so there should be no competition in the meta-universe either. All that
counts, according to Smolin, is that the type of universe that has the highest fecundity
is the winner:
It must also be stressed that at this formal level, concepts like survival of the fittest or
competition for resources play no role. What matters is only that rate of reproduction varies
strongly.29
A general emergence theory might help to focus the question of cosmic origins and
evolution, but selection theory only applies to biological systems where differential
reproduction is possible. And in fact a closer reading of Smolin reveals something
more akin to emergence than selection; the birth of a cosmos, for example, is a
bounce. Also, in complex systems, new collective effects emerge (including cosmic
symbioses), and, in extreme cases of disequilibration, evolution is rapid until new
stability is achieved.30 Though he acknowledges that conventional treatments of
selection theory emphasize competition, an important theme of evolution might be
the ability to invent new ways of living, in order to minimize the actual competition
among the species.31 But then he lets Richard Dawkins justify his adoption of a selec-
tionist stance:
The theory of evolution by natural selection is the only theory we know of that is, in principle,
capable of explaining the existence of organized complexity. Even if the evidence did not favor
it, it would still be the best theory available.32
Thus Smolin commits to natural selection as a universal law, going as far as to equate
evolution with the history of selection. But since competition and survival of the
fittest do not enter his thesis at any level, what he is really proposing is a cosmologi-
cal theory of fecundity. Moreover, what he finds interesting about evolution is
progressive self-organization, which despite Dawkins is an issue distinct from selection
theory. The Life of the Cosmos, and its review that I cited earlier, illustrates what a
tangled web ultra-Darwinism can weave. As ever, Monkey is free to roam at will,
provided he stays in the hand of Darwin, or perhaps Dawkins.
When James Lovelock portrayed Earth, or Gaia, as an evolving organismic whole,
Richard Dawkins objected that since Gaia had never been in competition with others
of its type, natural selection had no part in its development, and so, by definition, it
could not have evolved.33 The emergentist interpretation is that the absence of inter-
planetary competition meant that the only obstacles to Gaia becoming more complex
and self-organized were its physical limitations, and the stases in its biological systems.
It has gone through periods of emergent biospheric change, such as the conversion to
an oxygenated atmosphere, and the emergence of complex ecosystems that interact in
a planetary homeostasis, disrupted and reorganized by occasional contingencies such
as asteroid hits. Gaia also has the potential to reproduce, by sending out space habitats
and terraforming the other planets. But without that ever happening, it can be seen
to have auto-evolved, in the sense of having generated life, whose biomass has
increased and become more ordered, in the absence of competing Gaias. The Gaia
concept also reinforces the idea that dynamic stability can be changed, both progres-
sively and regressively. Such changes can be saltatory, as when a major bolide makes
an impact, or they can be critical-point emergences, as when the gradual accumula-
tion of atmospheric oxygen reaches the threshold where animals can leave the water
and occupy the land. Since humans can effect such major changes, we have to take
care in deciding what kind we want.
Metaphysical Aspects of Emergence

The following aphorism is J. B. S. Haldanes:
The fact about science is that everyone who has made a serious contribution to it is aware, or very
strongly suspects, that the world is not only queerer than anyone has imagined, but queerer than
anyone can imagine. This is a most disturbing thought, and one flees from it by stating the exact
opposite.34
Is it not time that we confronted that queerness and tried to understand it instead of
fleeing from it? The aphorism suggests why it has taken us so long to accept some
version or other of a comprehensive theory of biology, instead of one that equates
evolution with stasis. There are two poles that attract different kinds of extremists: one
lot flees from mystery, by operating as if the world is neither queer nor complex. Like
Democritus, they prefix their pronouncements with the phrase nothing but atoms
and the void (or molecules and genes). The nothing-but reductionists may have
fled from fear of the unknown, but they have also fled toward a strategic metaphysi-
cal position where they dominate not only biological philosophy but also command
most of the practical resources of biology. Their evangelical zeal nearly comes full
circle, resembling the romantic extreme of transcendental holism, which celebrates
complexity for its mystery. Emergentists, or realistic holists, or interactionists, if I
guess their responses correctly, celebrate the unknown for the challenge of under-
standing it. Any scientists who feel a warm glow at the realization that they do not
have the slightest inkling of how to explain the problem nature has just set them, will
appreciate this. In contrast, fleeing from the queerness of the universe, or sheltering it
from investigation by pretending that it is simple or irrelevant, will certainly prolong
the journey to the next level of understanding.
432 Chapter 11
Another potential philosophical value of emergentism was appreciated by C. L.

Prosser, one of the most influential comparative physiologists of the twentieth
century. While he unfortunately did not elaborate on emergent systems in physiology
and ecology, he thought they had a deep metaphysical power equivalent to that of
categories like beauty and valuenot a notion to inspire reductionists.35 In the same
vein, Brian Goodwin proposes an emergentistic science of qualities. Among human
emergent qualities he counts harmonious, self-regulating (as opposed to authoritative)
societies, holistic medicine, and play, all of which have strong subjective or uniquely
individual features. Wisdom, as an emergent quality of human individuals, and, one
would hope, their libraries and teachers, does not exist at the lower levels. Yet ultra-
Darwinism suggests that wisdom, along with human acts of systematic murder, rape
with malice aforethought, militarism, and other aspects of the will to power were
already programmed into the genes, and hence into behavioral algorithms, by the end
of the Pleistocene, through the action of natural selection. By their argument, our best
option is to be nobly objective, and not to hide from the conclusion that our evolu-
tionary success has depended on these genetically predetermined features, which must
be acknowledged and transcended. Any kind of nastiness can be rationalized in this
way, although some who buy the argument are the first to demand that we take the
miscreants and lock em up, then hang em high! The more insidious philosophical
sin is to diminish our values in order to validate our prejudices.
Emergentism does not promise a gentler and kinder universe; only a more thorough
realistic, holistic analysis. There are many benign emergent properties of the human
organism, such as aesthetic enjoyment and creativity, empathy and mystical
awareness, together with more objective abilities of logical and empirical analysis,
judgment, experience, memory and communicative skill. But, as Arthur Koestler
pointed out, they can be overridden by mass adherence to an emergent ideology.
People who are individually pacific can collectively go marching off to war (global or
guerilla), to perform acts that to call subhuman demeans the rest of the animal
kingdom.36 The structure of our behavior is not genetically determined. Nevertheless,
benign human qualities emerged out of archaic neural structures and ancient
hormonal ferments that can still rise to swamp them, often through a positive
feedback amplification triggered by social stimuli. This emphasizes the urgent need for
a true evolutionary psychology that does not beg the question that all behavior is the
genetically determined product of natural selection.
One small gain for emergentism could be the realization of Jenningss hope for a
release from accusations of anthropocentrism, when we talk about unique emergent
advances in human evolution, and emergence to higher levels of organization in
general. These evolutionary steps can be characterized in a variety of ways, including
number of differentiated cell types, and the complexity of supervening levels of coor-
dination. To say that the human is higher does not disparage the worm, but implies
that perfection-of-adaptation-to-environment is a totally inadequate assessment.

Jenningss hope for release from reductionism is also realized. Hylozoism claims that
all features of complex organisms, having gradually accumulated, must be found to a
degree in the simplest organisms. To the contrary, innovations that occur at each
emergence have new properties that did not exist before.
Quantity, Quality, and Subjectivity

Goodwins science of qualities is an admirable goal. Unfortunately, historic fear of
unknown qualities that might harbor vitalism, transcendentalism or intelligent
design, has driven the popularity of simplistic and intolerant reductionism. Design has
also been sanitized as a popular selectionist metaphor; but of course we all know
what such language really means. Quantitative rigor has become an end in itself, to
be substituted for qualitative observation, scrutiny of basic premises, and speculative
induction. It is easily applied to the big questions, but it is anti-intellectual if cases
where it is not as easily applied are dismissed as tiny and uninteresting. Here we can
reply Yes to the question Even if it makes a difference, does it matter? If we require
our students to prioritize quantifiability for their research proposals, we block all of the
interesting and original observations that might be made in the field. Precise quantifi-
cation must be secondary to identifying quality, and figuring out how it comes into
being. Is there a metaphysician in the house? An ontological diagnosis, please!37
Can we make anything of C. L. Prossers suggestion that the schism between
subjective and objective worldviews might be bridged by the insight of emergentism?
Consider the difference between mind and intelligence, difficult enough to define
objectively, though we try. Intelligence is a general term for an emergent property
of a brain whose protein structure is genetically determined and anatomy genetically
based. However, its development is modified by experience, and differs significantly at
the level of neuronal connections, even in genetically identical twins. Mind is the
larger subjective package of intelligence, together with education, memory, sensuous-
ness, consciousness, and subconscious activity. During the entire life of the individual,
feedback between mind and dynamic neuroendocrinal structure results in the modifi-
cation of both.
Why do humans do what they do? The constellation of mental properties
represented by the word mind are not gene-determined. Nor can they be, if mind is
to be adaptable, conferring a freedom of thought from traditional conditioning that
makes intellectual progress difficult. This we can contrast with the stereotyped
behavior patterns of insects and birds that have been strongly reinforced through
natural selection. In humans, an analogous mechanism of repression and regression
reinforces obedience to tradition. In recognizing that, emergentism has one hopeful
ontological quality. By demonstrating that biological evolutionary progress can be
made, despite the self-correction of stasis and its obstacles to change, it holds out some
434 Chapter 11
hope for theoretical progress as well. Mind is naturally highly subjective, even
solipsistic. As Michael Polanyi argued, the closest that we can ever come to objectivity
is a personal knowledge that has been subject to all of the structure and modification
of our heredity, experience, education and social conditioning.38 Doctrinaire reduc-
tionism is a flight from such subjectivity. There is plenty to be afraid of, doctrinaire
reductionism for example. But that is the price of imagination and creativity.
Emergentists and their predecessors often had a nose for ineffable qualities like vital
force and animal magnetism, many of which were finally identified and measured
because suspicion of their reality persisted until experimental validation became
technically possible. Cognition and freedom of thought are other such vital forces.
The invention of some kind of artificial intelligence that will explain mind mechanis-
tically, without resort to semantic reductionism is still an open question. One of the
emergent properties that it would need to display is the subjective flash of insight that
catalyzes change. That is a quality that gives a new meaning to social butterflies like
Confucius, Buddha, Moses, Jesus, Mohammed, Darwin, Marx, and Einstein, who
fluttered by with new ideas and rearranged the flowers on a global scale.
As Koestler pointed out in The Act of Creation (1964), intellectual emergent
properties have multiple manifestations in the humanities, arts and sciences, and not
the least of these properties is humor. Jokes mimic creative insight, making us laugh
at the bisociation of the punch line, and at ourselves for letting the narrative deliber-
ately lead us astray. Nature does not mislead us; we are quite capable of doing it to
ourselves, until parts that seemed dissociated converge and emerge as mental wholes.
And we laugh at our own inability to see it before. Out of all that individual subjectiv-
ity comes productive thought, both qualitative and quantitative. And, if we know that
emergences (both mental and evolutionary) are part of reality, we know that the end
of biotic evolution is not nigh, and that we should continue to expectand respect
surprises.39
I began this journey by identifying a need to understand the progressive evolution
of biological persistence out of the emergent properties of life: self-maintenance, and
reproductionsimple enough to say! Now I am back where I started, knowing that we
still have not explained how life itself emerged with those properties, nor how mind
emerged from them. We cannot depend on the discovery of a universal formulation
for emergence in all its manifestations since new rules are generated at every level and
are influenced by improbable contingencies. John Holland (1998) consoles us with the
thought that in any system that runs long enough, unlikely persistent patterns will
emerge. They are then candidates for combination with other persistent patterns, to
emerge as larger patterns with enhanced persistence. His closing question for future
study is, essentially, How do they do it? He cautions that the Baconian approach of
gathering data until significant relations emerge is unlikely to work because systems
exhibiting emergence are so complex.40
The latter warning came too late for me to heed. In any case, a Baconian study of
the interactive arenas of biology gave me a modus operandi that provides multiple
examples of the generative processes of association and repetitive differentiation (or
modularity). It also clarifies the particulars of the intrinsic and extrinsic causes of the
two fundamental types of emergent evolution: critical-point and saltatory. The com-
prehensive Baconian approach includes contingencies within the category of extrinsic
causes and so makes it possible to synthesize all the aspects of emergent evolutionary
causation. The need to explain the generative processes of evolution, to grant a central
role for repetitive differentiation, to accommodate saltatory events, and to include
extrinsic and intrinsic causes has been intuitively obvious to some evolutionists for
more than a century, so I have actually been engaged in analyzing hypotheses to
which others had already leapt. Nevertheless, I hope that my case histories have
contributed to an understanding of how wholes not only have properties that do not
exist in the parts, but also how such wholes come into existence. They cant but fail
to do so.
Millennial ideas about the end of progress and the end of science are popular
these days.41 Ever since Aristotle, we have suffered in every generation from the hubris
of scientists who think that they have most of it sorted out. Some biologists believe
that Darwin already had evolution all ship-shape and Bristol-fashion in The Origin of
Species. Darwin knew otherwise, but he had high hopes for the differences that his
theory would make to biology:
When we no longer look at an organic being as a savage looks at a ship, as at something wholly
beyond his comprehension; when we regard every production of nature as one which has had a
history; when we contemplate every complex structure and instinct as the summing up of many
contrivances, each useful to the possessor, nearly in the same way as when we look at any great
mechanical invention as the summing up of the labour, the experience, the reason, and even the
blunders of numerous workmen; when we thus view each organic being, how far more
interesting, I speak from experience, will the study of natural history become!
A grand and almost untrodden field of inquiry will be opened, on the causes and laws of
variation, on correlation of growth, on the effects of use and disuse, on the direct action of
external conditions, and so forth.42
Darwin went on to suggest future revelations from systematics, breeding experiments,

and the study of archetypal body forms through paleontology and embryology. All
have been realized in varying degrees. And there is no question that he did make the
study of natural history far more interesting. On the other hand, the fields mentioned
in his second paragraph remain almost untrodden, perhaps because summing up
is an inadequate way of synthesizing evolution. During the passage of Darwinian
Theory through the Modern Synthesis to ultra-Darwinism, Darwins unknowns of
evolution have been cast away for being too neo-Lamarckist or too saltatory. What
remains is little more than a hulk of contrivances, tingles, and dubious new ladings.
436 Chapter 11
The organism is still regarded as savages would have seen a ship. Analyzing its bits of
wood and nails and sails does not lead to the realization that the ship is greater than
the sum of its parts.
A theory of emergence, and its synthesis with selection theory, are hopeful episte-
mological monsters. Whether as ideas or organisms, rough beasts have always
slouched along the track of evolution.43 It would not have happened without them.
Now that humans are able to manipulate future evolution there will be rougher still.
But if we continue to canonize natural selection we will tread too much the dark side
of the path. I would hope that after the stasis of the twentieth century, a nascent,
generative theory of emergent evolution, and a general biological synthesis, would
help to carry Darwins program forward. T. S. Eliot reassures us that some ideas have a
greater destiny than their termination as meaningless husks:
What we call the beginning is often the end

And to make an end is to make a beginning.
The end is where we start from. . . .
We shall not cease from exploration
And the end of all our exploring
Will be to arrive where we started
And know the place for the first time.44
Notes
Introduction
1. Williams 1966, p. 139.
2. Endler 1986, p. 51.
3. Goodwin 1994, p. 531.
4. Hawkes 1997, p. 14.
5. The phrase Big Bang of Biology was popularized by the newsweekly Time in its issue of
December 4, 1995. It had earlier been used in Scientific American by J. S. Levinton (1992).
6. Grass 1977, p. 5. This is the English edition of the original 1973 publication in French.
7. Wilson 1970, p. 369, citing Lyells journal entries of March 1860.
8. Aristotle referred to the rungs on the ladder of life as hypostases. See Lovejoy 1936.
9. Gould 1989, p. 154, citing Conway Morris 1977. Hallucigenia was presented as a creature that
walked on spines and had dorsal tentacles. At first sight Conway Morris took it to be a bit of
something else. Now he has turned it upside-down, making the tentacles legs, and identifying it
as a kind of arthropod (Conway Morris 1998). Complexity theorists call bizarre experiments
kludges.
10. Von Bertalanffy 1967, p. 82.
11. Darwin 1872, p. 60.
12. Szalay 1998, p. 342 (emphasis added here).
13. Muir and Howard (1999) warn that transgenes used in genetically modified food organisms
might turn out to be such Trojan genes.
14. Bertalanffy 1952, p. 92.
15. Dobzhansky et al. 1977, p. 153.
16. Darwin 1859, p. 490. This was unchanged in the sixth edition of Origin, but Darwin had
hedged on p. 95: It is, however, an error to suppose that there would be no struggle for existence,
438 Notes to Introduction
and, consequently, no natural selection, until many forms had been produced: variations in a
single species inhabiting an isolated station might be beneficial, and thus the whole mass of
individuals might be modified, or two distinct forms might arise. He should have left well
enough alone.
17. Gould 1991.
18. The use of high table as a metaphor for the self-appointed elite of evolutionism is
attributed by Eldredge (1995) to Maynard Smith.
19. According to Adams (1979), the term gene pool was introduced by Dobzhansky (1950) and
popularized by Mayr (1963).
20. Gerhardt and Kirschner 1997, p. 205.
21. Mackie 1999. My colleague prefers to be called a Darwinist rather than a neo-Darwinist. The
insertion of God willing into his discourse is a tongue-in-cheek response to a reviewer of
Gerhart and Kirschner 1997 who wondered if the cubomedusan eye was evidence against the
existence of God. The debate emphasizes my point that natural selection has been a secular
replacement for the creator and that both require a certain degree of faith.
22. Bryan Sykes is leader of the group that analyzed the mitochondrial DNA of Cheddar Man. In
Sykes 1999, he puts Cheddar Man in a larger context of European human ancestry.
23. For a useful elaboration of this, see Moss 2003.
24. The phrase blanket utility is from Baldwin 1896.
25. Wimsatt 1998, p. 271.
26. Gould 1983c, p. 152.
27. Therefore, the way of life and the exploratory behavior of organisms may initiate adapta-
tional changes.
28. For a comparison of cosmological and biological evolution, see chapter 11.
29. This is paraphrased from an account of a Muller lecture by his graduate student (later my
professor of genetics) Guido Pontecorvo (Cohen 1997).
30. Muller 1949.
31. One of the first people I find to have used experiment in this sense was Max Delbrck
(1949). For fuller treatments of the uses and abuses of figurative language in biology, see Arber
1954, Oyama 1985, and Keller 1995.
32. Desmond and Moore 1991, p. 420f.
33. When I was writing Evolutionary Theory: The Unfinished Synthesis (1985), J. A. Shapiro had
already used this molecular biological metaphor. He later extended the idea in his essay Natural
genetic engineering in evolution (1992).
Notes to Chapter 1 439
34. Zambryski 1988, 1989.
35. Maynard Smith and Szathmry 1995, p. 8.
36. Ibid., p. 145.
37. One reader of my manuscript thought I might be criticized for my assumed superiority in
taking the high road. The metaphor is drawn from the song Loch Lomond, in which the low
road is by far the preferable route; the high road is death by hanging.
38. The expression art of the possible was applied by Herophilos to medicine in the fourth
century B.C.
39. Williams 1966, p. 139.
Chapter 1
1. Eldredge 1995, p. 36f. I ask his indulgence for reversing his order of march.
2. Berry 2000, p. 117.
3. In Darwin 1872, see p. 60 for natural selection as a false term and p. 47 for a power
incessantly ready for action, and as immeasurably superior to mans feeble efforts as the works of
Nature are to those of Art.
4. Darwin 1872, p. 392.
5. In Evolutionary Theory: The Unfinished Synthesis (1985a, p. 144ff.), I discuss the objections that
were raised against the reductionism of cell theory by the organismalists. These objections were
ignored by the next generation of reductionists who were to out-reduce the cell theorists by
making DNA the lowest common denominator of life.
6. For discussions, see Greene 1971; Shapere 1971; Mayr 1974.
7. My historian colleague Judith Friedman volunteered this opinion about evolutionary

paradigms prior to discourse about my own thoughts. For an earlier discussion, see Reid 1985a,
p. 107. In afterthoughts about scientific revolutions, Kuhn (2000) thought that the more gradu-
alistic model suggested by the Modern Synthesis could be closer to the truth than the
mutationist/revolutionist model. Alas, poor Yorick! I thought I knew him.
8. Poulton 1908, p. 97.
9. Goudge 1961.
10. Cope 1887.
11. Wallace 1858, p. 60.
12. Schmalhausen 1949, p. 53.
13. The example of grassfinch behavior is from pp. 593594 of Futuyama 1998. It was brought
to my attention by Camilla Berry, whose comment is cited from p. 60 of her 2000 thesis. Robert
440 Notes to Chapter 1
Wesson devotes a section of his 1991 book Beyond Natural Selection to the caprices of creative
selection pressure.
14. Williams 1966, p. 34.
15. Ibid., p. 255f.
16. Cohen and Stewart 1997, p. 136.
17. Horgan (1996, p. 255) uses theological Darwinians. Horgan vacillates on his own
adherence to this faith. On natural selection in the guise of creator, see Skolimowski 1974 and
Paterson 1982.
18. Schwartz 1999, p. 304f.
19. Ruse 1996, p. 493.
20. Ibid., p. 331.
21. Smocovitis (1996), citing Provine 1992.
22. Mayr 1980, p. 40, also citing Laudun 1977.
23. Ibid., p. 40.
24. Many a paradigm buff must have thought of this line. I thought John Casti (1989) had
priority for using it as a book title, but a search of the Internet reveals that it is polyphyletic.
25. Kuhn 1970, p. 6.
26. Ibid., p. 67f.
27. I borrow this image from Eldredge (1995, p. 4). Eldredge calls it High Table, an expression
attributed to J. Maynard Smith. To avoid mixing my thematic nautical metaphor, I prefer
captains table, which still conveys the sense of privilege, elitism, etc. Eldredge perceives that
paleontologists have received reluctant invitations to join the company at the table, but that
does not make it any less elitist since epigeneticists, physiologists and those who research
symbiosis and evolution are conspicuous by their absence.
28. Kuhn 1970, p. 88.
29. See Goodwin in Brockman 1995, p. 105.
30. Campbell 1993, p. 494.
31. Endler 1989, p. 51.
32. Ibid., p. 97.
33. Dawkins 1976.
34. One of the best current discourses in favor of the importance of organismal and the
inadequacy of selfish gene concepts is developed by David Rollo (1995). The word phenotype
is unfortunately corrupted by its genocentric definition as an expression of the genotype. See also
Dover 2000.
35. Darwin 1872, p. 107.
36. Clark 1975, p. 99, translating Spinozas Ethics III. 7.
37. Shapere 1980, p. 393.
38. Hamburger 1980, p. 99f.
39. Arthur 1997, p. 218, citing Horder 1994.
40. Nagel 1978, chapter 13.
41. Wallace, as cited by Mivart (1871) on evolution of mind.
42. Mivart 1871, p. 313. Mivart borrowed Galtons metaphor of a multifaceted stone that would
roll or stay put according to the energy applied.
43. Herbert Spencer (1862), cited by Oldroyd (1980, p. 205).
44. Mivart 1871, p. 113, citing Galton. Punctuated equilibrium was described by a waggish
gradualist as evolution by jerks, but Eldredge (1995) exacts a fine revenge. Eldredge (1985) and
Gould (2003) reassess punctuated equilibrium.
45. Keller 1983.
46. Mayr 1954.
47. Kimura 1960.
48. Ohno 1970, preface.
49. Butler 1886.
50. Lincoln et al. 1998. This idea comes from Van Valen (1965).
51. Darwin 1859, p. 41.
52. Wallace 1858, p. 61.
53. Darwin 1872, p. 59.
54. Kolesnikova 1987.
55. Belyaev died in 1985. For a summary of his Russian publications, see Sumnyj and Ruvinskij
1987. See also Belyaev and Trut 1987. For a list of Belyaevs English publications, see Jablonka and
Lamb 1995.
56. E. Darwin 1794, p. 320f. See also McNeil 1987, p. 104.
57. For a succinct discussion of Mayrs treatment of proximate and ultimate causes, see pp. 7779
of Cor van der Weele 1999.
58. Mayr 1991, p. 145.
59. Van der Weele 1999, citing Mayr 1994.

60. Williams 1966, p. 4.
61. Ibid., p. 5.
62. Ibid., p. 270f.
63. Ibid., p. 55.
64. Dawkins, in Brockman 1995, p. 48. Re Biblical misquotation: In John 8:12, Jesus refers to
himself as the light of the world. This is often mixed up with John 14:6 I am the way, the truth
and the lifeodd how the truth was left out by Wilson (1998b, p. 60) and Williams (1966, p.
273). Jesus himself may have misremembered his quotes; see Job 38:19 Where is the way where
light dwelleth?
65. Steve Jones, in Brockman 1995, p. 95.
66. On Luther and reason, see Honderich 1995, p. 514.
67. Eldredge 1995, p. 226.
68. Bacon 1620, p. 5.
69. Lvtrup 1975, p. 511.
70. This quotation from the bacteriologist Melvin Cohn is borrowed from p. ix of Bibel 1992,
which attempts a synthesis in some ways more ambitious than the present work. A bacteriologist
and an immunologist, Bibel is the kind of rare bird mentioned by her source. I find it reassuring
that there are other biologists who are not afraid to go naked in the market place. She does not
detail the source of the quotation.
71. Bateson 1894, p. 13.
72. Ibid., p. 13.
Chapter 2
2. Holland 1998, p. 1.
3. On natural selection as book-keeping, see Wimsatt 1980.
4. See, for example, Brooks and Wiley 1986 and Prigogene and Stengers 1984.
5. Conrad 1990, p. 79.
6. Ibid., p. 61.
7. Kauffman 1992, p. xiv.
8. Wilson 1998b, p. 60.
9. See note 67 to chapter 1.

10. Woodger 1929, p. xv.
11. Goodwin 1994, p. xi.
12. This seems to be the equivalent of hierarchical reductionism (Dawkins 1989).
14. Ibid., p. 228.
15. Ibid., p. 376.
16. Ibid., p. 380.
17. Kim (1999, p. 33), citing Galen (~200 A.D.) On The Elements According to Hippocrates 1. 3. 70:
1574. p. 23.
18. Drummond 1883, p. 405.
19. Alexander 1920, p. 46f.
20. Holland 1998, p. 190.
21. Morgan 1931, p. 5.
22. Bak and Kan Chen 1991; Bak 1996.
23. Caudwell 1986, p. 176. Foster (2000) explains that the British Communist Party, which had
published Caudwells other works, held back Development and Heredity because its emergentism
seemed too idealistic. Engels, on the other hand, had too many political commitments to see The
Dialectics of Nature published promptly. His Anti-Dring (1878) was the only hint of his
emergentism in the meantime.
24. Sperry 1983, p. 79.
25. Oyama 2000, p. 181f. Note also that Cohen is the biologist and Stewart is the mathematician
in their collaborative authorship of The Collapse of Chaos (1994).
26. Kauffman 1995, p. 23.
27. Holland 1998, p. 239.
28. Corning 1998, p. 11.
29. El-Hani and Pihlstrm 2002, p. 30.
30. Dawkins (1995, p. 83) lays claim to the question of the evolution of evolvability.
31. Benford (1995, p. 136) uses the phrase The Enormous Emergence. The quotation is from p.
274 of Martin and Benford 1996.
32. Otte and Endler 1989.
33. Lovelock (1988) is a proponent of geophysiology.

34. Biologists are forever arguing about teleology and might be suspicious of goal-directed
activities. What I mean is any series of specific related actions that terminates at a predetermined
pointsometimes called teleonomic, as distinct from teleological. It may be the final product
of a biochemical pathway, the healing of a wound by clotting and tissue regeneration, or a
sequence of behaviors. For a discussion, see pp. 278282 of Reid 1985a.
35. Dobzhansky 1967, p. 58. Dobzhansky attributes the idea of a unique, emergent humanum to
Brunner (1952).
36. Ibid., p. 57.
37. Ibid., p. 61.
38. Gehring 1998, p. 99.
Chapter 3
1. Margulis 1981, p. 201.
2. Margulis 1998, p. 8.
3. Jennings 1927, p. 22.
4. Margulis 1981, pp. 222224.
5. Margulis 1998, p. 11.
6. Sapp and I probably share a quirky appreciation of the word-play parallel between our title and
the idiom guilt by association. While acknowledging his outstanding contribution to the
subject, I will not plead guilty to plagiarism, since I have been using this title for seminars since
1986, and I used it in an abstract published in 1987.
7. Sapp 1994, p. 131f.
8. Sapp (1994, p. 159) refers to the Wollmans unpublished inferences on paraheredity.
9. I use Meyer-Abichs 1964 coinage to draw attention to his little appreciated contribution to
symbiosis studies.
10. Fitt 1985.
11. On aspects of lichen symbioses, see Douglas 1994, pp. 15, 17, 5152.
12. Aristotle, De Motu Animalium.
13. Aristotle, Politics; De Motu, 703a29f.
14. Heddi et al. 2001, citing Perru 1997.
15. Haines 2002.
16. Aksoy 2000

17. Buchner 1965; Clark et al. 2000.
18. See the review by Boursaux-Eude and Gross (2000).
19. Yoshida et al. 2001.
20. Fukatsu and Ishakawa 1993.
21. Imms 1957, p. 800.
22. Dohlen et al. 2001.
23. Curtis and Walter 1995.
24. Caetano and Da Cruz-Landim 1985, cited by Boursaux-Eude and Gross (2000).
25. On leafcutter ants, see Van Borm et al. 2002. They also survey the status of ant symbioses in
general.
26. Currie et al. 1999, cited in Boursaux-Eude and Gross 2000.
27. Reviewed by Haines 2002, citing Morin et al. 2000.
28. Marcotrigiano 1999.
29. Cohen (2001), interviewing Luis Villarreal of the University of California at Irvine; Muir et
al. 2004.
30. Greider 1998.
32. Cavalier-Smith 1985.
33. Edelman 1987.
34. Reid 1985a, p. 144ff.
35. Jennings 1927, p. 22.
36. Wilson 1975, p. 7.
37. Shostak and Kolluri 1995.
38. Rudman 1981.
39. Pirozynski and Malloch 1975.
40. Douglas 1994, p. 19.
41. Maser et al. 1978.
42. Margulis 1981, citing Cleveland and Grimstone 1964.
43. Margulis 1981, p. 12.
44. Klenk et al. 1997.

45. Martin and Mller 1998.
46. Doolittle 1998.
47. Ibid.
48. Margulis and Sagan (2002) base these assumptions on the work of R. Gupta.
49. Margulis and Sagan 2002, p. 158.
50. Martin and Mller 1998.
51. Niklas 1997, p. 133f.
52. Ibid., p. 143.
53. Sapp 1994, p. 40.
54. Ibid., p. 185, citing Uzell and Spolsky 1974.
55. Schwartz and Dayhoff 1978.
56. Margulis 1981, p. 18f.
57. Bryant et al. 1998.
58. Fankboner and Reid 1981.
59. Reid 1990.
60. Douglas 1994, p. 54.
61. Tatewaki et al. 1983
62. Margulis and Sagan, 2002, p. 60f.
63. Bry et al. 1996; Hooper et al. 2001
64. Fankboner 1971.
65. Douglas 1994, pp. 101103.
66. The definitions set out here are to be found in chapter 2 of Wilson 1975.
67. Costerton et al. 1995
68. England et al. 1999; Dunny and Wians 1999.
69. Shimkets 1990; Dworkin 1996.
70. Burkholder 1999.
71. Bever and Simms 2000.
72. Shapiro 1998.
73. Engelberg-Kulka and Glaser 1999.

74. Crespi 2001, p. 182.
75. Virchow 1858. This refers to his major work. For a summary of his preliminary opinions on
the cell theory, see Hall 1969, volume 2, p. 280ff.
76. Sol and Goodwin (2000, p. 149) recommend the more extensive comparisons of societies
and neural organization made by Gordon et al. (1992) and Gordon (1999).
77. I may be putting words into the mouths of Sol and Goodwin here, but this is what their
comparison means to me.
78. Whewell 1840, cited in Wilson 1998b, p. 8.
Chapter 4
1. Murphy 1869, p. 68. Nicely said, but the French physiologist Milne Edwards promoted the
idea of a division of physiological labor in 1834.
2. Child 1924, p. 43.
3. J. Huxley 1942, p. 564f. As I argued in chapter 1, it was Huxleys sensitivity to the importance
of such progressive evolution that put him beyond the pale of the Modern Synthesis that he
helped to create.
4. Woodger 1929, p. 41.
5. Darwin 1859, p. 141.
6. Darwin 1872, p. 349.
7. Arthur 1997, pp. 287289.
8. Bernard, strictly speaking, was not post-Darwinian, but his most important work was done
after the publication of The Origin of Species. The physiologist Viscount J. S. Haldane (father of J.
B. S. Haldane) was fixated on the holistic aspects of physiology, but did not focus strongly on
how it evolved. See Reid 1985a, p. 109f.
10. Whytes early ideas on the subject were formulated before he encountered Schmalhausens
book, and although the parallels are remarkable he gave it short shrift. As well as having priority,
Schmalhausens biological treatment was the more substantial. On Whytes contribution and the
broader historical context of physiological organization, see chapter 14 of Reid 1985a.
11. Rollo 1994, p. 256.
12. Conrad 1990, p. 79.
13. Conrad 1983, p. 10.

14. Harbo 1997. My interest in this species began with honours thesis research by my student
Mia Parker in 1995. I then made additional informal studies of ecological distribution and
feeding behavior, some of which are published here for the first time.
15. Rollo 1994, citing and paraphrasing Alexander 1991, p. 446.
16. I believe Bernard first made his frequently quoted comment La fixit du milieu intrieur;
cest la condition de la vie libre in a lecture given in 1872.
17. For a summary of the theories of Severtsov and Schmalhausen, see Adams 1980.
18. Waddington 1957.
19. Gould and Vrba 1982. This was a re-invention of the Funktionswechsels wheel (Dohrn 1875).
20. Schmalhausen 1949, p. 233. I have inserted my own translations of the words adaptation
and adaptive, since he used them less definitively than he might have. I suspect his original
Russian was more precise.
21. Darwin 1872, p. 135.
22. The full citation list for these studies includes Wynne-Edwards 1998; McMillan and Wynne-
Edwards 1998, 1999; and Wynne-Edwards et al. 1999.
23. Le Maho 1977.
24. Sherman et al. 1992.
25. Grmillet and Wanless 2000; Grmillet et al. 2005.
26. See De Beer 1940, p. 95.
27. For reviews of genetic assimilation, see Reid 1985a, Hall 2001, and West-Eberhard 2003b.
28. Woodger 1929, p. xv. The semantic reductions that I mentioned in the introduction are
epistemological intolerant abstractions.
29. For a useful review of the origin-of-life hypotheses, see Maynard Smith and Szathmry 1996.
30. Schueller 1998.
31. Ibid.
32. Orgel 1994.
33. Kauffman 1995, p. 50.
34. Ibid., p. 62.
35. Rebeck 1994.
36. Schwartzs ideas were obtained by means of a telephone interview. At the time of writing, his
intended book had not been published.
37. For the fundamental arguments, see Zuckerkandl 1975.

38. Kauffman 1995, chapter 4, p. 71ff.
39. See Ganti 1974 for chemotons and Woese and Fox 1977 for progenotes. See also the 1995
review by Maynard Smith and Szathmry.
40. Doolittle and Brown 1994.
41. Weng et al. 1999, p. 93.
42. Ibid., p. 94.
43. The literature is awash with neologisms that are redundant or misleading, or invented for
self-serving reasons. I am reluctant to compound these errors, preferring to resurrect the
historical name unless it is already redundant or misleading. Although the process is presently
known to molecular biologists as the production of variant repeats (see chapter 6), to call it
variant repetition puts the cart before the horse.
44. Hochachka (1973) reviews his salmonid kinase research.
45. Ohno 1970, p. i.
46. Britten and Davidson 1971.
47. Pray 2004.
48. Wallis 1996.
49. Jiminez et al. 1993.
50. Li and Graur 1991, p. 80, citing Goodman 1981 and Czelusniak et al. 1982.
51. Segre and Goldring 1993.
52. Gerhart and Kirschner 1997, p. 223.
53. Fleming and Allison 1922.
54. Gerhart and Kirschner 1997, p. 204, citing Wistow 1993.
55. Newcombe et al. 1997, cited by Lewontin 2000, p. 117.
56. Mangum and Towle 1977.
57. Hochachka 1973.
58. On photosynthesis evolution, see Niklas 1997.
59. Pearson 1986, p. 12.
60. Pearson 2004, p. 77.
62. Uvarov 1977. See also chapter 5 of the present volume.
63. Collins and Cheek 1983.

Chapter 5
1. Waddington 1957, p. 13.
2. Ho and Saunders 1982, p. 93.
3. Mller and Wagner 1991, p. 230.
4. Woodger 1929, p. 372.
5. Bacon et al. 2001. Its nice to see a historical and philosophical perspective on the subject.
Nevertheless, as in the original model, Socrates is the inevitable winner of the debate.
6. See Hall 1992 and Arthur 1997.
7. See chapters 1 and 4 re Belyaev (1970) on sports and on breeding programs that destabilize
epigenetic patterns.
8. Darwin 1859, p. 12; p. 21 for pigeons; p. 31 for the Sebright quotation.
9. Geoffroy 1826.
10. T. H. Huxley 1864, p. 34.
11. On Murphy and Mivart, see chapter 3 of Reid 1985a.
12. For appreciations of Cope, see Gould 1977a and Reid 1985a.
13. Brooks 1883.
14. Bateson 1928, p. 42f.
15. Reid 2003.
16. De Vries 19011903.
17. Spemann 1914.
18. Arthur 1998, p. 99, citing Spemann 1938, p. 367f.
19. E. B.Wilson (1928) had made the distinction between pragmatic experimenters and the more
romantic generalists.
20. Kukalova-Peck 1983.
21. Murray et al. 1981; Palka et al. 1983.
22. Rollo 1994, p. 105.
23. The role of neural crest cells in avian facial prominences was confirmed for chicken embryos
by Le Livre (1978), Noden (1983), and Couly et al. (1998). Lee et al. (2001) show the subsequent
involvement of bone morphogenetic protein and retinoic acid.
24. For example, see Lloyd 1984.

25. West-Eberhard 1989, p. 256f. For a more extensive treatment of this subject, see West-
Eberhard 2003b.
26. West-Eberhard 2003a; Larsen 2004.
27. Slijper 1942, summarized in West-Eberhard 1989. West-Eberhard provides more examples of
these kinds of change on p. 255 of the aforementioned work; she gives more details of the goat
case in West-Eberhard 2003b.
28. Waddington 1969, p. 221.
29. Saunders 1984, p. 255.
30. Garstang, one of several biologists interested in radical changes in invertebrate development,
also distinguished himself by writing about them in verse (1951). See Hall 2000 on Garstang and
De Beer, and also on the earlier, nowadays overlooked work of the developmental evolutionist
Frank Balfour, a student of Ray Lankester and a teacher of Bateson and Weldon.
31. Hardy 1965, p. 217.
32. Gerhart and Kirschner 1997, pp. 331ff. On chronological expression of Hox, see Gilbert 1997,
chapter 16.
34. Mller 1990, p. 121.
35. Ibid., p. 109.
36. Ibid., p. 104.
37. Ibid. Mller cites Long 1976 and Brylski and Hall 1988 on cheek pouches.
38. Carroll (1988) and Burke (1989) on the subject of the sudden evolution of the chelonid
carapace, cited by Mller (1990, p. 107).
39. Raff and Wray 1989, Raff et al. 1990, and Wray and Raff 1990, cited in Muller and Wagner
1991, p. 234.
41. On the developmental evolution of bird skeletons, see Mller 1989, 1991.
42. Futuyama 1998.
43. Mller 1991.
44. Newman and Mller 2000.
45. All quotations in this paragraph from Keller 2002, p. 252, citing Dassow et al. 2000. See also
Meir et al. 2002.
46. Hall 2001, p. 219.

47. Osborn 1896, p. 312.
48. Kane 1995.
49. Darwin 1871, p. 119f.
50. Waddington 1942.
51. West-Eberhard 2003b, p. 147.
52. Wake 1989, 2003.
53. This is an unpublished observation regarding an unidentified species of the Orchestia type in
Haida Gwaii (Queen Charlotte Islands) of British Columbia. Since both beach and sea levels went
up and down like a pair of unsynchronized yo-yos in the wake of the last glaciation
(Hetherington et al. 2002), Matsuda may have been right on both counts.
54. Referenced on pp. 107109 of van der Weele 1999.
55. Newman and Mller 2000, p. 305, citing Magee 1997.
56. Ibid., p. 305, citing Deeming and Ferguson 1988.
57. Ibid., p. 305, citing McLaren and Michie 1958.
58. Balon 1983 and 1986; see also Bruton 1994.
59. Oyama 2000, p. 39.
60. Garstang 1922, p. 81, cited in Hall 2000.
61. Newman and Mller 2000, p. 303.
62. Ibid., p. 305.
63. Brenner 1972; Sulston et al. 1980; Wood et al. 1988.
64. Hill et al. 1992, p. 60, cited in Gehring 1998.
65. Gehring 1998, p. 204, quoting calculations made by Rubin.
66. Newman and Mller 2000, p. 307, citing Kazmierczak and Degens 1986.
67. Newman (1994) includes epiboly, involution and delamination. See Steinberg 2003 for a
more comprehensive account of differential adhesive reactions.
68. Goodwin 1989, p. 92.
69. Newman and Mller 2000, p. 307, citing the formation of lumens in tumors (Tsarfaty et al.
1992).
70. Nsslein-Volhard 1996, p. 61. This author points out that the importance of gradients was
emphasized by Boveri a century ago. See also Haraway 1976.

72. Newman and Mller 2000, p. 307, citing Palmeirim et al. 1997 and Newman 1993. See also
Nsslein-Volhard 1996.
73. This paraphrases Newman and Mller 2000, p. 310, citing various authors.
74. Frey et al. 1997.
75. I discuss the controversial usage of goals in Reid 1985a.
Chapter 6
1. Campbell 1985, cited by Jablonka and Lamb 1994, p. 72.
2. Matsuda 1987, p. 53.
4. Woodger 1929, p. 32. Woodger probably borrowed this construction from G. K. Chesterton.
5. The cuisine metaphor is borrowed, with thanks, from an unpublished essay on epigenetics by
my former student Kevin Little. It pops up in the literature in such a way as to suggest poly-
phyletic origins.
6. Novick and Weiner 1957, cited in Jablonka and Lamb 1994, p. 82.
7. Johnston 2004.
8. Wolffe and Matzke 1999. The verbal communication metaphor is Kevin Littles (personal com-
munication).
9. Pelling 1959; Clever and Karlson 1960.
10. Baker 1997.
11. Li and Graur 1991, p. 159.
12. Tittiger et al. 1993.
13. Li and Graur 1991, p. 15.
14. Li and Graur 2000, p. 294f.
15. Nowak 1994.
16. Li et al. 2001.
17. Lewin 1997, p. 525ff.
18. See Caporale 2003, p. 86ff. She notes also that the acronym SOS (Save our ship) was
suggested by Miroslav Radman, a molecular biologist with a family background in fishing.
19. On HR and NHEJ, see Lin and Waldman 2001 and Willet-Brozick et al. 2001.
20. Pirkkala et al. 2001 is a good general reference for heat-shock proteins.
21. Brenner et al. 1993; see also Elgar et al. 1999.
22. Jablonka and Lamb 1994, p. 69f.
23. Prody et al. 1989.
24. These examples are from Jablonka and Lamb 1994 and Prody et al. 1989.
25. Moxon and Wills 1999.
26. King 1994; King, Soller, and Kashi 1994.
27. Moxon and Wills 1999, p. 99.
28. Wurtele et al. 2003; Little and Chartrand 2004.
29. Lin and Waldman 2001; Willett-Brozick et al. 2001.
30. Li et al. 2001.
31. Lachmansingh and Rollo 1994.
32. Baker 1997, p. 101.
33. Laudet et al. 1992 Laudet 1999.
34. For a brief history of concerted evolution, see Graur and Li 2000, p. 304ff. See also Dover
2000.
35. Dover 1982, p. 111.
36. Li and Graur 1991, p. 164.
37. Ibid., p. 166.
38. Ibid., p. 140f.
39. Graur and Li 2000, p. 290f.
40. Li and Graur 1991, p. 188.
42. Li and Graur 1991, p. 193f.
43. Hurst and Randerson 2002.
44. Starr and Cline 2002.
45. Ting et al. 1992.
46. Gerhart and Kirschner 1997, pp. 309314.
47. Walter Gehring (1998) gives a remarkable account of the recent history of this research, in
which he played a leading role.
48. Raff (1996), discussing the work of Kukalova-Pek (1983).
49. Kukalova-Pek 1983.
50. Carroll 1995, p. 482.
51. Ibid., p. 481.
52. Ronshaugen et al. 2002
53. For additional references, see Carroll 1995, p. 483.
54. Gerhart and Kirschner 1997, pp. 532535.
55. Burke et al. 1995, cited by Carroll 1995.
56. Tomarev et al. 1997.
57. Experiments with eyeless were conducted in 1994 in Gehrings laboratory. Gehring credits
Gerry Rubin with the calculation that 2,500 genes are involved in eye construction.
58. Gerhardt and Kirschner 1997, p. 205. George Mackies (1999) response is also cited in the
introduction to the present work.
59. Goodwin 1994, p. 167f. He does not use the term generative conditions of emergence, and
I have expanded these beyond those that he cites.
60. Behe 1996, p. 41.
61. Gould 1983n, p. 186, citing Darwin 1868.
62. Grimes and Aufderheide 1991, cited by Jablonka and Lamb 1994, p. 87. Also Jablonka and
Lamb 1994, p. 89.
63. Jablonka and Lamb 1994, p. 90.
64. Ibid., p. 102.
65. Monk 1995.
66. Surani 2001.
68. Pray 2004, p. 1.
69. Jablonka and Lamb are, however, conspicuous by their absence from Prays references.
70. Jablonka and Lamb 1994, p. 232, citing Bottema 1989.
72. Arthur 1997, pp. 5463; Wray 1998.
73. Jablonka and Lamb 1994, p. 171f.

74. Jegalian and Lahn 2001, p. 58. See also Lahn and Page 1997, 1999; Jegalian and Page 1998.
75. Dover 2000, p. 108ff.
76. Wells 1813.
77. Shapiro 1992, p. 101f.
78. Yuh and Davidson 1998.
79. Driever and Nsslein-Volhard 1988a,b.
Chapter 7
1. Darwin 1872, p. 157.
2. Eimer 1898, p. 467.
3. Waagen 1867; Haake 1895. See Bowler 1979 and Reid 1985a.
4. Goldschmidt 1940, p. 22.
5. J. Huxley 1942, p. 304f., citing Watson 1926.
6. Eldredge 1995, p. 129ff.
7. The pull of the present metaphor is used by Raff (1996, p. 129).
8. Simpson 1944, p. 150.
9. Ibid., p. 155.
10. Thompson 1941, p. 807f.
11. Ibid., p. 1094f.
12. Reid 1985a, p. 199. At the time I had overlooked Bowler 1979 and Grehan 1984. Mea maxima
culpa! Thanks to John Grehan for a gentle nudge.
13. Grehan and Ainsworth (1985) regarding Dovers response to orthogenetic implications of
molecular drive (1982).
14. Arthur 1997, p. 213.
15. Britten and Davidson 1971, p. 118.
16. Lima-De-Faria 1988, p. 211, citing Ritossa et al. 1971, Tartof 1974, Brown and Dawid 1968,
and Perkowska et al. 1968. See also Jablonka and Lamb 1995, p. 70.
17. Vrba 2004 and personal communication.
18. Gould 1974.
19. On Triceratops see Gerhard and Kirschner 1998, p. 551. For a survey of the range of effects of
neural crest organizer cells on head anatomies, see ibid., pp. 552554.
20. On the theoretical significance of horse allometry, see Eldredge 1995, p. 129ff.
21. Thomson 1992, p. 136.
22. Ibid., p. 136.
23. Ibid., p. 137.
24. Raff 1996, p. 25.
25. Ashitawa et al. 1994.
26. On Huntingtons disease see Rubinsztein et al. 1994. On fragile-X pathology see Parrish et al.
1994. I am most grateful to the biological historian Judith Friedmann for priming me on the
subject of anticipation.
27. Ashitawa et al. 1994.
28. Dover 2000, p. 101.
29. Ibid., p. 209.
30. Ibid., p. 32.
31. For a review of the RNA experiments see Eigen and Schuster 1979.
32. Brown et al. 2004; Morwood et al. 2004.
33. Fondon and Gardner 2004, p. 18060.
34. Ibid., p. 18061.
Chapter 8
1. Vrba 1989, p. 382.
2. Kauffman 1995, p. 23.
3. Gould 1996, in Horgan 1996, p. 124f.
4. Kauffman 1993, p. 180.
5. See also Reid 1985b.
6. Mayr 1960, p. 249. I have already mentioned Darwins musings on generative variability.
7. Mayr 1960, p. 351. Some developmental evolutionists have tried to distinguish between major
innovation and trivial novelty. That I do find stultifying.
8. Ibid., p. 364.
9. Ibid., p. 364.
10. Relevant publications from the Brenowitz group include Smith et al. 1997 and Tramontin et
al. 1998.
11. Mayr 1960, p. 368.
12. Ibid., p. 369.
13. Ibid., p. 371.
14. Ibid., p. 377.
15. Ibid., p. 371.
16. Ibid., p. 374.
17. Darwin 1872, pp. 112, 365.
19. I am grateful to my colleague John Taylor for some material used here. See also Taylor and
Raes 2005.
20. Maynard Smith 1988, p. 222.
21. Ibid., p. 222f.
22. Rollo 1994, p. 8.
23. Riedl 1978, p. 110.
24. Ibid., p. 272.
25. Ibid., p. 117.
26. Ibid., p. 126.
27. Ibid., p. 127.
28. Ibid., p. 129.
29. Ibid., pp. 132138.
30. Vrba and Eldredge 1984, p. 146.
31. Vrba 1989, p. 382.
32. Ibid., p. 390.
33. Salthe 1985, p. 155.
34. Ibid., p. 201.
35. Campbell 1993, p. 5. I refer to the third edition. Although I am aware its success has resulted
in subsequent editions, these generalities about evolution have not changed, despite the fact that
the 1999 fifth edition, co-authored with Reece and Mitchell, chose Dawkins as the key
interviewee on evolution.
36. Ibid. 1993, p. 7.

37. Polanyi 1958, p. 151f.
39. Ibid., p. 243.
40. Ibid., p. 242.
41. Ibid., p. 245.
42. Ibid., p. 251.
44. Ibid., p. 441.
45. Kauffman 1993, p. xiv.
46. Ibid., p. xv.
47. Ibid., p. xvi.
48. Holland 1998, p. 222ff.
49. Ibid., p. 125ff.
50. Ibid., p. 225.
51. Ibid., p. 227.
52. Ibid., p. 229.
53. Wimsatt 1997, p. S376.
54. Ibid., p. S382.
55. Corning 1998 p. 23.
56. Ibid., p. 15f.
57. Wynne-Edwards 1962. Corning (1997) singles out D. S. Wilson (1975 and subsequent publi-
cations) as the leader of the attempt to bring back group selection.
58. Morowitz 2002, p. 104f.
59. Frey et al. 1997.
60. J. Schwartz 1999, p. 342.
61. Bakker hints at this function in his seminal 1975 paper in Scientific American.
62. Bak and Chen 1971.
63. Kauffman 1993, p. xv.
64. On locusts, see Uvarov 1977. On cannibalism in salamanders, see Collins and Cheek 1983
and Maret and Collins 1997; see also Hall 1999, p. 303.
65. Rollo 1994, p. xii.
66. Kauffman 1993, p. xvii.
67. Raup 1986, p. 22.
Chapter 9
1. I have slightly abbreviated this version of Bacons Novum Organum, without, I hope, losing any
of his original intentions (Bacon 1620; p. 82 in my 1901 edition).
2. Darwin wrote entangled for his renowned final paragraph in the first edition of Origin. My
sixth edition says tangled, but this may be a printers error.
3. Piaget 1968.
4. Piaget 1979, p. 23. A similar notion about behavioral innovation in the absence of natural
selection had been expressed by R. Chauvin (1977).
5. Mller 1990, p. 123f. This authors assertion in point 6, regarding plasticity at all developmen-
tal levels, anticipates Kirschner and Gerharts (2005) emphasis on epigenetic adaptability and
exploratory behavior during development.
6. Mller and Wagner 1991, p. 234. I have paraphrased their citations of Raff and Wray 1989 and
Raff et al. 1990.
7. Ibid., p. 235, citing Wake and Roth 1989.
8. Bateson (1888) in a letter to his sister Anna, cited on pp. 4243 of Bateson 1928.
9. Wimsatt 1998, p. 270.
10. Wimsatt 1999, p. 142.
11. See, e.g., Little and Chartrand 2004.
12. Balon, cited by Bruton 1994, p. 271. See also Balon 1986.
13. Balon 1983, p. 2049.
14. See Hooper et al. 2001 on bacterial commensals of mammals and Tatewaki et al. 1983 on
epigenetic effect of bacteria on thallus-formation in Ulva and related green macroalgae.
15. West-Eberhard 2003b.
16. Lewontin 2000, p. 48.
17. See www.kakaporecovery.org.nz/involved/reading.html.
18. Turner 2000, p. 213.
19. Lamarck 1809 I, p. 267.
20. Kobayashi and Inaba 2000.

21. Lovelock 1988, p. 10. Huttons two papers on The theory of the earth were read to the
Royal Society of Edinburgh in 1785, and published in its proceedings in 1788.
22. McNeil 1987.
23. Ring 1982. For a review of the cold adaptations and cold adaptabilities of Arctic insects, see
Ring and Tesar 1981.
24. Darwin 1859, p. 489f.
25. See Vendruscolo and Dobson 2005; Trinh Xuan Hoang et al. 2004; Chotia et al. 2003.
26. Dohrn 1875; Gould and Vrba 1982.
27. Bacon 1620, p. 82. See also his New Atlantis (1628) on the division of scientific labor.
Chapter 10
1. Lamarck 1809 I, p. 221.
2. J. Huxley 1942, p. 578.
3. Holland 1998, p. 231.
4. J. Huxley 1942, p. 568.
5. West-Eberhard (2003b) uses the expression phenotypic plasticity for the latter properties.
However, although her treatment of the subject is comprehensive, phenotypic plasticity in earlier
and narrower neo-Darwinist applications is a misnomer equivalent to the taxonomists nomen
nudum: i.e., a name that cannot be used because as originally published it failed to meet
taxonomic standards; in the case of phenotypic plasticity, failure to meet the explicit meaning of
the word plasticity!
6. Brenner 1999, p. 1964.
7. Anderson 1994, cited by Sol and Goodwin 2000, p. 18.
8. Sol and Goodwin 2000, p. 13ff.
9. Rollo 1994, p. 14.
10. J. Huxley 1942, p. 571.
11. Popper 1972.
12. Beament 1961.
13. Waldrop 1992, p. 288.
14. Horgan 1996, p. 206.
15. Holland 1998, p. 231.
16. Personal communication from Tom Reimchen, University of Victoria.

17. Newman and Mller 2000, pp. 304 and 315 respectively.
18. Valentine 1986.
Chapter 11
1. T. S. Eliot, Little Gidding, in Four Quartets (1943).
2. Vrba and Eldredge 1984, p. 146.
3. Jennings 1927, p. 22.
4. Science 293 (2001), p. 1086.
5. Keller 2002, p. 254.
6. Reid and Brand 1986; Reid 1990, 1998.
7. I should temper this conclusion by noting that the studies in question did provide morpho-
logical details from which valid inferences could be made about the symbiosis, regardless of their
original interpretation.
8. Ronshaugen et al. 2002.
9. Kukalova-Peck 1983.
10. Grant and Grant 1994.
12. Ibid., p. 553.
13. Mungo is a bred-in-captivity parrot whose acquisition was prompted by the original work of
Irene Pepperberg with Alex, her African grey. See Pepperberg 1998.
14. Stebbins, 1987 lecture at Cornell University, cited in Grene 1988, p. 55.
15. Re Stiassny and Meyer 1999, p. 3.
16. Ibid., p. 68.
17. Ibid., p. 69.
18. Fryer and Iles 1972; Greenwood, 1974; Stiassny 1991; Stiassny and Meyer 1999.
19. Stiassny and Meyer 1999, p. 66.
20. Paterson 1985.
21. Grene 1988, p. 68.
22. Leroi 1998, p. 82.
23. Provine 2001, p. 204.

24. Lotka 1922.
25. Chaisson 2001, p. 216.
26. George Herbert (15931633), popularized by Benjamin Franklin (1758). See pp. 270 and 374
of Bartletts Familiar Quotations (1980).
27. Linde 1994. Horgan (1996, pp. 98102) discusses his views.
28. Dyer 1997.
29. Smolin 1997, p. 104.
30. Ibid., p. 150f.
31. Ibid., p. 185.
32. Ibid., p. 105f, citing Dawkins The Blind Watchmaker; no page reference given.
33. Cohen and Stewart (1994, p. 375) attribute this criticism to Dawkins. Sheri Tepper (1998)
gives an interesting fictional account of a Gaian superorganism that has complexified to the
point of having intelligent and semi-independent subunits that lack sexual reproduction,
depending instead on cooperation with the parental whole to persist.
34. Clark 1968, citing a letter from Haldane to Robert Graves.
35. Prosser 1965, p. 364.
36. Koestler 1967, p. 349.
37. My philosopher friend C. B. (Danny) Daniels, a movie buff, has waited in vain to see the
question Is there a metaphysician in the house? flashed on the screen. I hereby indulge him
and thank him for his reflections on Spinoza, single-malts, and oysters on the half-shell.
38. Polanyi 1958.
39. Peirce 1898.
40. Holland 1998, p. 242.
41. Gunther Stent (1969) started the trend in biology a bit early for the millenium, though it is
obvious from his use of Robert Frosts It Is Almost the Year Two Thousand as an introductory
quotation that he had the millenium in mind. John Horgan (1996) took up the refrain. I am not
sure that he actually believes that the end of science is nigh, but I got a lot of mileage out of his
discourse in any case.
42. Darwin 1859, p. 485f.
43. The rough beast is the hopeful monster in The Second Coming (Yeats 1920).
44. Eliot 1943.

Bibliography
After I published Evolutionary Theory: The Unfinished Synthesis, I returned to my

research on mollusks. After ten years, no saltatory emergences had occurred in evolu-
tionary theory, and a chance encounter with Brian Goodwin and David Lambert in
Auckland goaded me to return to the fray.
I would like to acknowledge some works that I found particularly stimulating on my
re-entry to the lists. The first group includes, in the order in which I encountered
them, Stephen Jay Goulds 1994 Scientific American essay The evolution of life on
Earth, David Rollos Phenotypes: Their Epigenetics, Ecology and Evolution (1994), Eva
Jablonka and Marion Lambs Epigenetic Inheritance and Evolution: The Lamarckian
Dimension (1995), Antonio Lima-de-Farias Evolution without Selection: Form and
Function by Autoevolution (1988), Niles Eldredges The Reinvention of Darwin (1995), Jack
Cohen and Ian Stewarts The Collapse of Chaos (1994), and Stuart Kauffmans At Home
in the Universe (1995). John Horgans The End of Science (1996) was also provocatively
stimulating. I am not in complete agreement with these authors views of evolution-
ary theory, since they all allow themselves to be bogged down by natural selection. (It
operates that way in theory as well as in nature.) Nevertheless, I have great respect for
their talents and freely admit their positive influence upon me.
Publications of conference and workshop proceedings leave far too much space
between the stools that the important stuff can fall into. Nevertheless, I found
Matthew Niteckis University of Chicago series, in particular Evolutionary Progress
(1988) and Evolutionary Innovations (1990), to be useful. And I have to confess to
personal contributions to the 1988 American Zoological Societys symposium Is the
Organism Necessary and to the 2001 KLI workshop on Ryuichi Matsuda and eco-
evo-devo, where I met strangers who seemed like old friends immediately.
Although Brian Goodwin had hinted darkly to me about the contents of his book
How the Leopard Changed Its Spots before its publication, I did not catch up with it until
I had finished my first draft. But his 1989 essay Evolution and the generative order
had already had a catalytic effect, and How the Leopard Changed Its Spots later precipi-
tated some of my thoughts into a more solid form.
466 Bibliography
Of all the major works on the subject of complexity by authors who start from the
bottom, I found John Hollands Emergence: From Chaos to Order (1998) the most
valuable for comparative purposes, and more often on my side of the Looking Glass
than not. Although I like to work in a state of enlightened ignorance, to avoid con-
structing a pastiche of other peoples ideas that would hinder the development of my
own, I probably should have taken a fuller account of Susan Oyama from the outset.
Furthermore, I have not specified here the numerous works by Lynn Margulis and her
co-author Dorion Sagan that have emerged along the rocky road of symbiosis theory.
But I was already intellectually charged by her ideas long before I conceived of the
present work.
In the time between my submission of the final manuscript and the copy-editing
stage, several important books appeared. I have minimally mentioned some of them
in the text. They include Callebaut and Raskin-Gutmanns Modularity: Understanding
the Development and Evolution of Natural Complex Systems, Jablonka and Lambs
Epigenetic Inheritance and Evolution: The Lamarckian Dimension, and Kirschner and
Gerharts The Plausibility of Life: Resolving Darwins Dilemma, all published in 2005. In
a planned future volume that will deal with the history of life as envisioned by an
emergentist, I expect to give the latter works fuller consideration, as well as Mller and
Newmans Origination of Organismal Form: Beyond the Gene in Developmental and
Evolutionary Biology.
I have received much reference material from so many colleagues, correspondents,
and students that I am unable to name them all; some of their names appear in the
endnotes. But a general thank you is in order.
I have listed the first editions of books, followed by the editions whose pages I have
cited.
Adams MB (1979) From gene fund to gene pool: On the evolution of evolutionary language.
Studies in the History of Biology 3: 241285.
Adams MB (1980) Severtsov and Schmalhausen: Russian morphology and the evolutionary
synthesis. In The Evolutionary Synthesis, ed. Mayr E, Provine W. Cambridge: Harvard University
Press.
Adler MJ (2001) A novel mechanism for evolution? Science 294: 53.
Aksoy S (2000) Tsetsea haven for microorganisms. Parasitology Today 16: 114118.
Alexander RD (1991) Some unanswered questions about naked mole rats. In The Biology of the
Naked Mole-Rat, ed. Sherman P, Jarvis J, Alexander R. Princeton: Princeton University Press.
Alexander S (1920) Space, Time and Deity. London: Macmillan.
Alt FW, Kellems RE, Bertino JR, Schinke RT (1978) Selective multiplications of dihydrofolate
reductase genes in methotrexate-resistant variants of cultured murine cells. J. Biol. Chem. 253:
13571370.
Bibliography 467
Altmann K (1890, 1894) Die Elementerorganismen und ihre Beziehungen zu den Zellen. Leipzig:
Von Veit.
Anderson PW (1994) A Career in Theoretical Physics. Singapore: World Scientific Publishing.
Appel TA (1987) The Cuvier-Geoffroy Debate: French Biology in the Decades before Darwin.
Oxford: Oxford University Press.
Arber A (1954) The Mind and the Eye. Cambridge: Cambridge University Press.
Arthur W (1997) The Origin of Animal Body Plans: A Study in Evolutionary Developmental
Biology. Cambridge: Cambridge University Press.
Arthur W (1998) The emerging conceptual framework of evolutionary developmental biology.

Nature 415: 757764.
Ashby WR (1952) Design for a Brain. New York: Wiley.
Ashizawa T, Anvret M, Baiget M, Barcelo JM, Brunner H, Cobo AM, Dallapiccola B, Fenwick RGG,
Grandell W, Harley H, Junien C, Koch MC, Korneluk RG, Lavedan C, Miki T, Mulley JC, de
Munian AL, Novelli G, Roses AD, Seltzer WK, Shaw dJ, Smeets H, Sutherland R, Yamagata H,
Harper PS (1994) Characteristics of intergenerational contractions of the CTG repeat in myotonic
dystrophy. Am J. Human Genetics 54: 414423.
Babbage C (1838) The Ninth Bridgewater Treatise: A Fragment, second edition. London: Murray.
Bacon F (1620) Novum Organum. London. 1902 edition, New York: Collier.
Bacon M, Wu C-T, Morris J (2001) Genes, genetics, and epigenetics: A correspondence. Science
293: 11031105.
Bak P (1996). How Nature Works: The Science of Self-Organized Criticality. New York: Springer.
Bak P, Chen K (1991) Self-organized criticality. Sci. Am. 264, January: 4653.
Baker MW (1997) Steroid receptor phylogeny and vertebrate origins. Molecular and Cellular
Endocrinology 135: 101107.
Bakker R (1975) Dinosaur renaissance. Sci. Am. 232, July: 5878.
Baldwin JM (1896) A new factor in evolution. Am. Nat. 30: 354536.
Baldwin JM (1897) Organic selection. Nature 55: 558.
Balon EK (1983) Epigenetic mechanisms: Reflections on evolutionary processes. Canadian

Journal of Fisheries and Aquatic Sciences 40: 20452058.
Balon EK (1986) Saltatory ontogeny and evolution. Rivista di Biologia Biology Forum 79:
151190.
Balon EK (l989) The epigenetic mechanisms of bifurcation and alternative life-history styles. In
Alternative Life-History Styles of Animals, ed. Bruton M. Dordrecht: Kluwer.
Balon EK (2004) Alternative ontogenies and evolution: A farewell to gradualism. In Environment,

Development and Evolution, ed. Hall B, Pearson R, and Mller G. Cambridge: MIT Press.
Bardou F, Jaeger L (2004) Large phenotype jumps in biomolecular evolution. Physical Review E
69: 031908-1031908-7.
468 Bibliography
Barrie VJ, Conway KW (2002) Rapid sea level change and coastal evolution on the Pacific margin
of Canada. J. Sedimentary Geol. 150: 171183.
Bartlett J (1980) Bartletts Familiar Quotations, fifteenth edition, ed. Beck E. Boston: Little, Brown.
Bateson B (1928) William Bateson F.R.S. Cambridge: Cambridge University Press.
Bateson W (1894) Materials for the Study of Variation, with Especial Regard to Discontinuity in
the Origin of the Species. Cambridge: Cambridge University Press. Reprinted by Johns Hopkins
University Press, 1992.
Beament JW (1961) The role of physiology in adaptation and competition between animals.
Symp. Soc. Exptl. Biol. 15: 6271.
Beament JW (1964) The active transport and passive movement of water in insects. In Advances
in Insect Physiology, volume 2, ed. Beament J, Treherne J, Wigglesworth V. Academic Press.
Beard DB, Dotson EM, Pennington PM, Eichler S, Cordon-Rosales C, Durvasula RV (2001)
Bacterial symbiosis and paratransgenic control of vector-borne Chagas disease. International
Journal for Parasitology 31: 621627.
Beardsley T (1997) Evolution evolving. Sci. Am., September: 1516.
Behe MJ (1996) Darwins Black Box. New York: Simon and Schuster.
Bell G (1988) Sex and Death in Protozoa: The History of an Obsession. Cambridge: Cambridge
University Press.
Belyaev DK (1969) Domestication of animals. Sci. J. 1: 4752.
Belyaev DK (1979) Destabilizing selection as a factor in domestication. Journal of Heredity 70:

301308.
Belyaev DK, Trut LN (1989) The role of behaviour in the evolutionary organization of wild
animals into domestic forms. In Behaviour as One of the Main Factors of Evolution, ed.
Leonovicov V, Novk V. Prague: Czechoslovak Academy of Sciences.
Benford G (1995) Sailing Bright Eternity. New York: Bantam Spectra.
Benveniste RE (1985) The contributions of retroviruses to the study of mammalian evolution. In

Molecular Evolutionary Genetics, ed. MacIntyre R. New York: Plenum.
Berg LS (1926) Nomogenesis or Evolution Determined by Law. London: Constable. First

published in Russian in 1922. English edition reissued in 1969 by MIT Press.
Berg R (1988) Acquired Traits. New York: Viking Penguin.
Bergson H (1908) Lvolution cratrice. Paris: Alcan.
Bernard C (1878) Leons sur les phnomnes de la vie, communes aux animaux et aux vgtaux.
Paris: Baillire.
Berry CV (2000) Bulldogs, Watchdogs and Underdogs: Is Evolutionary Theory a Paradigm or a

Kennel? MSc thesis, University of Victoria, B.C.
Bertalanffy L von (1952) Problems of Life. New York: Wiley.

Bibliography 469
Bertalanffy L von (1967) Robots, Men, and Minds. New York: Braziller.
Bertalanffy L von (1968) General System Theory. New York: Braziller.
Bestor TH, Chandler VL, Feinberg AP (1994) Epigenetic effects in eukaryotic gene expression.
Developmental Genetics 15: 458462.
Beurlen K (1930) Vergleichende Stammesgeschichte, Grundlagen, Methoden, Probleme, unter

besonderer Berucksiehtigung der hoheren Krebse. Fortschr. Geol. 7: 317586.
Bever JD and Simms EL (2000) Evolution of nitrogen fixation in spatially structured populations
of Rhizobium. Heredity 85: 366372.
Bibel DJ (1992) Freeing the Goose in the Bottle: Discovering Zen through Science, Understanding
Science through Zen. Oakland, CA: Elie Metchnikoff Memorial Library.
Bolk L (1929) The origin of racial characteristics in man. Am. J. Phys. Anth. 13: 128.
Bonner JT (1974) On Development. Cambridge: Harvard University Press.
Bonner JT (1988) The Evolution of Complexity by Means of Natural Selection. Princeton:

Princeton University Press.
Bottema S (1989) Some observations on the modern domestication processes. In The Walking
Larder, ed. Clutton-Beck J. London: Unwin Hyman.
Boursaux-Eude C, Gross R (2000) New insights into symbiotic associations between ants and
bacteria. Res. Microbiol. 151: 513519.
Bowler PJ (1979) Theodor Eimer. Evolution by definitely directed evolution. J. Hist. Med. Allied
Sci. 34: 4073.
Brenner SE (1974) The genetics of Caenorhabditis elegans. Genetics 77: 7194.
Brenner SE (1999) Theoretical biology in the third millenium. Phil. Trans. Roy. Soc. Lond. 354:
19631965.
Brenner SE, Elgar G, Sandford R, Macrea A, Venkatesh B, Aparicio S (1993) Characterization of the
pufferfish (fugu) genome as a compact model vertebrate genome. Nature 366: 265268.
Breznac JA, Brune A (1994) Role of microorganisms in digestion of lignocellulose by termites.

Ann. Rev. Entomology 39: 453488.
Britten RJ, Davidson EH (1969) Gene regulation for higher cells: A theory. Science 165: 349357.
Britten RJ, Davidson EH (1971) Repetitive and non-repetitive DNA sequences and a speculation
on the origins of evolutionary novelty. Quart. Rev. Biol. 46: 111138.
Brockman J (1995) The Third Culture: Beyond the Scientific Revolution. New York: Simon and
Schuster.
Brooks DR, Wiley EO (1986) Evolution as Entropy: Toward a Unified Theory of Biology. Chicago:
University of Chicago Press.
Brooks WK (1883) The Law of Heredity: A Study of the Cause of Variation, and the Origin of
Living Organisms. Baltimore: Murphy.
470 Bibliography
Brown DD, David IB (1968) Specific gene amplification in oocytes. Science 160: 272280.
Brown DD, Wensink PC, Jordan E (1972) A comparison of the ribosomal DNAs of Xenopus laevis
and Xenopus mlleri: Evolution of tandem genes. J. Mol. Biol. 63: 5773.
Brown P, Sutikna T, Morwood MJ, Soejono RP, Jatmiko, Septomo EW, Rokus AD A new small-
bodied hominin from the Late Pleistocene of Flores, Indonesia. Nature 431: 10551061.
Brunner E (1952) The Christian Doctrine of Creation and Redemption. New York: Westminster.
Bruton MN (1994) The epigenesis of an epigeneticist: An interview with Eugene Balon. South
African Journal of Science 90: 270275.
Bry L, Falk PG, Midtvedt T, Gordon JI (1996) A model of host-microbial interactions in an open
mammalian ecosystem. Science 273: 13801383.
Bryant D, Burke L, McManus J, Spalding M (1998) Reefs at Risk. Washington: World Resources
Institute.
Brylski P, Hall BK (1988) Ontogeny of a macroevolutionary phenotype: The external cheek

pouches of geomyoid rodents. Evolution 42: 391395.
Buchner P (1965) Endosymbiosis of Animals with Plant Micro-organisms. New York: Wiley
Interscience.
Burke AC (1989) The development of the turtle carapace: Implications for the evolution of a
novel bauplan. J. Morphology 199: 363378.
Burke AC, Nelson CE, Morgan BA, Tabin CL (1995) Hox genes and the evolution of vertebrate
axial morphology. Development 121: 333346.
Burkhardt RW (1977) The Spirit of System: Lamarck and Evolutionary Biology. Cambridge:
Harvard University Press.
Burkholder JM (1999) The lurking perils of Pfiesteria. Sci. Am. 281, August: 4249.
Buss LW (1987) The Evolution of Individuality. Princeton: Princeton University Press.
Butler S (1879) Evolution Old and New. London: Hardwicke & Bogue.
Butler S (1886) Luck or Cunning. London: Fifield.
Cai H, Levine M (1995) Modulation of enhancer-promoter interactions by insulators in the

Drosophila embryo. Nature 376: 533536.
Cain AJ, Sheppard PM (1954) Natural selection in Cepaea. Genetics 39: 89116.
Cairns-Smith AG (1971) The Life Puzzle. Edinburgh: Oliver and Boyd.
Callebaut W, Rasskin-Gutman D, eds. (2005) Modularity: Understanding the Development and

Evolution of Natural Complex Systems. Cambridge: MIT Press.
Campbell JH (1985) An organizational interpretation of evolution. In Evolution at a Crossroads,

ed. Depew D, Weber B. Cambridge: MIT Press.
Campbell NA (1993) Biology, third edition. Redwood City, CA: Benjamin/Cummings.
Campbell NA, Reece JB, Mitchell LG (1999) Biology, fifth edition. Menlo Park, CA:
Benjamin/Cummings.
Bibliography 471
Cannon WB (1932) The Wisdom of the Body. New York: Norton.
Caporale LH (2003) Darwin in the Genome: Molecular Strategies in Biological Evolution.

McGraw-Hill.
Caporale LH (2003) Natural selection and the emergence of a mutational phenotype: An update
of the evolutionary synthesis considering mechanisms that affect genome variation. Ann. Rev.
Microbiol. 57: 467485.
Carroll L (1867, 1887). Alice through the Looking Glass. Reissued by Folio Society, London, 1962.
Carroll R (1988) Paleontology and Vertebrate Evolution. New York: Freeman.
Carroll R (1997) Patterns and Processes of Vertebrate Evolution. Cambridge: Cambridge

University Press.
Carroll SB (1995) Homeotic genes and the evolution of arthropods and chordates. Nature 376:
479485.
Casti J (1989) Paradigms Lost: Images of Man in the Mirror of Science. New York: Morrow.
Caudwell C (1986) Heredity and development. In Caudwell, Scenes and Actions. London:
Routledge and Kegan Paul.
Cavalier-Smith T (1985) The Evolution of Genome Size. Chichester: Wiley.
Cavalier-Smith T (1987) The origin of cells: A symbiosis between genes, catalysts and membranes.
Cold Spring Harbor Symp. Quant. Biol. 52: 805842.
Cavanaugh CM (1983) Symbiotic chemoautotrophic bacteria in marine invertebrates from

sulphide-rich habitats. Nature 302: 5861.
Chaisson EJ (2001) Cosmic Evolution: The Rise of Complexity in Nature. Cambridge: Harvard
University Press.
Chambers R (1844) Vestiges of the Natural History of Creation. London: Churchill. Reissued 1994
in facsimile by University of Chicago Press.
Chan WWS, Chong KY, Madinovich C, Simerly C, Schallen G (2001) Transgenic monkeys
produced by retroviral gene transfer into mature oocytes. Science 291: 309312.
Chauvin R (1977) Ethology: The Biological Study of Animal Behavior. New York: International
Universities Press.
Cheng G, Aksoy S (1999) Tissue tropism, transmission and expression of foreign genes in vivo in
midgut symbionts of tsetse flies. Insect Molecular Biology 8, 125132.
Child CM (1924) Physiological Foundations of Behaviour. New York: Holt.
Chothia C, Gough J, Vogel C, Teichmann SA (2003) Evolution of the protein repertoire. Science
300: 17011703.
Churchill FB (1980) The modern evolutionary synthesis and the biogenetic law. In The
Evolutionary Synthesis, ed. Mayr E, Provine W. Cambridge: Harvard University Press.
Clark MA, Moran NA, Baumann P, Wernegreen JJ (2000) Cospeciation between bacterial
endosymbionts (Buchnera) and a recent radiation of aphids (Uroleucon) and pitfalls of testing for
phylogenetic congruence. Evolution 54: 517525.
472 Bibliography
Clark R (1968) J.B.S.: The Life and Work of J.B.S. Haldane. London: Hodder and Stoughton.
Clark SRL (1975) Aristotles Man. Oxford: Clarendon.
Cleveland LR, Grimstone RV (1964) The fine structure of the flagellate Mixotricha paradoxa and
its associated micro-organisms. Proc. Roy. Soc. B159: 668686.
Clever U, Karlson P (1960) Induktion von Puff-Vernderungen in den Speicheldrsenchro-

mosomen von Chironomus tentans durch Ecdyson. Exp. Cell Res. 20: 623626.
Cohen B (1997) Genetics: A heritage of excellence. The Avenue (Glasgow University) 22: 2022.
Cohen J, Stewart I (1994) The Collapse of Chaos. New York: Penguin.
Cohen P (2001) Mothers little helper. New Scientist, February 24: 10.
Cole BJ (1991) Is animal behaviour chaotic? Evidence from the activity of ants. Proc. Roy. Soc.
B224: 253259.
Collins JH, Cheek JE (1983) Effect of food and density on development of typical and cannibal-
istic salamander larvae in Ambystoma tigrinum nebulosum. Amer. Zool. 23: 7784.
Conrad M (1983) Adaptability: The Significance of Variability from Molecule to Ecosystem. New
York: Plenum.
Conrad M (1990) The geometry of evolution. Biosystems 24: 6181.
Conway Morris S (1977) A new metazoan from the Burgess Shale. Paleontology 20: 623640.
Conway Morris S (1995) Ecology in deep time. Trends in Ecology and Evolution 10: 290294.
Conway Morris S (1998) The Crucible of Creation. Oxford: Oxford University Press.
Cook LM (1961) The edge effect in population genetics. Am. Nat. 95: 295307.
Cope ED (1887) The Origin of the Fittest. Chicago: Open Court
Cope ED (1896) The Primary Factors of Organic Evolution. Chicago: Open Court.
Copleston F (1960) A History of Philosophy. Modern Philosophy, volume 4: Descartes to Leibniz.

Birmingham: Newman. Garden City, NY: Doubleday Image Edition, 1963.
Corning PA (1997) Holistic Darwinism: Synergistic selection and the evolutionary process.
Journal of Social and Evolutionary Systems 20: 363401.
Corning PA (1998) The synergism hypothesis. On the concept of synergy and its role in the
evolution of complex systems. Journal of Social and Evolutionary Systems 21: 135.
Corning PA (2002) Natures Magic: Synergy in Evolution and the Fate of Humankind. Cambridge:
Cambridge University Press.
Costerton JM, Lewandowski Z (1995) Microbial biofilms. Annual Review of Microbiology 49:
711745.
Couly G, Grapin-Botton A, Coltey P, Ruhin B, Le Douarin NM (1998) Determination of the

identity of the derivatives of the cephalic neural crest: Incompatability between Hox gene
expression and lower jaw development. Development 125: 34453459.
Bibliography 473
Covello PS, Gray MW (1992) Silent mitochondrial and active nuclear genes for subunit 2 of
cytochrome oxidase (cox 2) in soybean: Evidence for RNA-mediated gene transfer. EMBO J. 11:
38153820.
Cremer T, Cremer C (2001) Chromosome territories, nuclear architecture and gene regulation in
mammalian cells. Nature Reviews Genetics 2: 292301.
Crespi BJ (2001) The evolution of social behavior in microorganisms. Trends in Ecology and
Evolution 16: 178183.
Croizat L (1962) Space, Time, Form: The Biological Synthesis. Caracas: Published by the author.
Cruse D (1999) Science and intentionality: Exploring a serious contradiction in the logic of
scientific materialism. Unpublished ms. received by R. G. B. Reid from the author.
Curtis AD, Waller DA (1997) Variation in rates of nitrogen fixation in termites: Response to
dietary nitrogen in the field and laboratory. Physiological Entomology 22: 303.
Cuthill S (1994) Cellular epigenetics and the origin of cancer. BioEssays 16 (6): 393394.
Czelusniak J, Goodman M, Hewett-Emmett D, Weiss ML, Venta PJ, Tashian RE (1982)

Phylogenetic origins and adaptive evolution of avian and mammalian haemoglobin genes.
Nature 298: 297300.
Darwin C (1859) On the Origin of Species by Means of Natural Selection. London: Murray.
Darwin C (1868) The Variation of Animals and Plants under Domestication. London: Murray.
Darwin C (1871) The Descent of Man. London: Murray.
Darwin C (1872) On the Origin of Species by Means of Natural Selection, sixth edition. London:
Murray.
Darwin E (1794) Zoonomia. Johnson. Third edition, 1801.
Darwin F, ed. (1892) The Autobiography of Charles Darwin and Selected Letters. London:
Appleton. Facsimile edition: New York: Dover, 1961.
Dassow GE von, Meir E, Munro GM, Odell M (2000) The segment polarity network is a robust
developmental module. Nature 406: 188192.
Davidson EH, Peterson KJ, Cameron RA (1995) Origin of bilaterian body plans: Evolution of
developmental regulatory mechanisms. Science 270: 13191325.
Davies P (1999) The Fifth Miracle. The Search for the Origin and Meaning of Life. New York:
Touchstone.
Daviss B (1998) Cast out of the Garden of Eden. New Scientist 158: 2630.
Davitaschvili L (1966) The Contemporary Status of Evolutionary Studies in the West (published
in Russian). Moscow: Acad. Sci. USSR, Div. Gen. Biol., Science Publ. House.
Dawkins R (1976) The Selfish Gene. Oxford: Oxford University Press.
Dawkins R (1982) The Extended Phenotype. Oxford: Oxford University Press.
Dawkins R (1985) The Blind Watchmaker. London: Longman.

474 Bibliography
Dawkins R (1989) The evolution of evolvability. In Artificial Life, volume 1, ed. Langton C.
Redwood City CA: Addison-Wesley.
Dawkins R (1995) A survival machine. In The Third Culture, ed. Brockman J. New York: Simon
and Schuster.
De Bary A (1879) Die Erscheinung der Symbiose. Vortrag auf der Versammlung der Naturforscher
und Artze zu Cassel. Strassburg: Trubner.
De Beer G (1940) Embryos and Ancestors. Oxford: Oxford University Press.
Deeming DC, Ferguson MW (1988) Environmental regulation of sex determination in reptiles.

Phil. Trans. Roy. Soc. B322: 1939.
De la Mettrie JO (1748) LHomme machine. Leiden.
Delbrck M (1949) A physicist looks at biology. Trans. Conn. Acad. Arts Sci. 38: 173190.
Desmond A, Moore J (1991) Darwin. The Life of a Tormented Evolutionist. New York: Norton.
Detera-Wadleigh SD, Fanning TG (1994) Phylogeny of the steroid receptor superfamily.

Molecular Phylogenetics and Evolution 3: 192205.
De Vries H (190103) Die Mutationstheorie. Leipzig: Von Veit.
De Vries H (190910) Mutation Theory. Chicago: Open Court.
Dobzhansky T (1937) Genetics and the Origin of Species. New York: Columbia University Press.
Dobzhansky T (1967) The Biology of Ultimate Concern. New York: New American Library.
Dobzhansky T, Ayala FJ, Stebbins GL, Valentine JW (1977) Evolution. San Francisco: Freeman.
Dohlen CD von, Kohler S, Alsop ST, McManus WR (2001) Mealybug -proteobacterial endosym-
bionts contain -proteobacterial symbionts. Nature 412: 433436.
Dohrn A (1875) Der Ursprung der Wirbelthiere und das Prinzip des Funktionswechsels:
Genealogische Skizzen.
Doolittle WF (1987) The origin and function of intervening sequences: A review. Am. Nat. 130:
915928.
Doolittle WF (1991) The nature of introns. Current Biol. UK 1: 145146.
Doolittle WF (2002) Microbial genomes multiply. Nature 416: 697700.
Doolittle WF, Brown JR (1994) Tempo, mode, the progenote and the universal root. Proc. Natl.
Acad. Sci. 91: 67216728.
Douglas AE (1994) Symbiotic Interactions. Oxford: Oxford University Press.
Dover GA (1982) Molecular drive: A cohesive mode of species evolution. Nature 299: 111117.
Dover GA (1986) Molecular drive in multigene families. How biological novelties arise, spread,
are assimilated. Trends in Genetics 2: 159165.
Dover GA (2000) Anti-Dawkins. In Alas, Poor Darwin: Arguments against Evolutionary

Psychology, ed. Rose H, Rose S. London: Jonathan Cape.
Bibliography 475
Dover GA (2000) Dear Mr. Darwin. Berkeley: University of California Press.
Driesch H (1908) The Science and Philosophy of the Organism. London: Black.
Driever W, Nsslein-Volhard C (1988a) The bicoid protein determines position in the Drosophila
embryo in a concentration-dependent manner. Cell 54: 8393.
Driever W, Nsslein-Volhard C (1988b) A gradient of bicoid protein in Drosophila embryos. Cell

54: 95104.
Drummond H (1883) Natural Law in the Spiritual World. London: Hodder and Stoughton.
Drummond H (1894) The Ascent of Man. London: Hodder and Stoughton.
Duchesne LC, Larson DW (1989) Cellulose and the evolution of plant life. BioScience 39:
238241.
Dworkin J, Allamonda LJ, Deamer DW, Sandford SA (2001) Self-assembling amphiphilic

molecules: Synthesis in simulated interstellar/precometary ice. Proc. Natl. Acad. Sci. 98: 815819.
Dyer G (1997) Darwin theory proving to be survival of fittest. Victoria Times Colonist, August 24.
Edelman GM (1987) Cell adhesion and the evolutionary origins of immunity. Immunological
Reviews 100: 1145.
Eimer T (1898) On Orthogenesis and the Impotence of Natural Selection in Species Formation.
Chicago: Open Court.
Eldredge N (1985) Time Frames: The Rethinking of Darwinian Evolution and the Theory of
Punctuated Equilibria. New York: Simon and Schuster.
Eldredge N (1985) Unfinished Synthesis: Biological Hierarchies and Modern Evolutionary

Thought. Oxford: Oxford University Press.
Eldredge N (1995) Reinventing Darwin: The Great Debate at the High Table of Evolutionary
Theory. New York: Wiley.
Eldredge N, Gould SJ (1972) Punctuated equilibria: An alternative to phyletic Gradualism. In

Models in Paleobiology, ed. San Francisco: Schopf T. Freeman, Cooper.
El-Hani CN, Pihlstrm S (2002) Emergence theories and pragmatic realism. http://www
.helsinki.fi/science/commens/papers/emergentism.pdf.
Eliot TS (1943) Little Gidding. In Four Quartets. New York: Harcourt, Brace.
Emerson AE (1939) Social coordination and the superorganism. Amer. Midl. Nat. 21: 182209.
Endler JA (1986) Natural Selection in the Wild. Princeton: Princeton University Press.
Engelberg-Kulka H, Glaser G (1999) Addiction modules and programmed cell death and
antideath in bacterial cultures. Ann. Rev. Microbiol. 53: 4370.
Engels F (1878) Anti-Dring. Leipzig.
Engels (1954) The Dialectics of Nature. Moscow: Foreign Languages Publishing. First published in
Russian and German in 1925.
Escriva H, Manzon L, Youson J, Laudet V (2002) Analysis of lamprey and hagfish genes reveals a
complexity of gene duplication during early vertebrate evolution. Mol. Biol. Evol. 19: 14401450.
476 Bibliography
Fankboner PV (1971) Intracellular digestion of symbiotic zooxanthellae by host amoebocytes in

giant clams (Bivalvia: Tridacnidae), with a note on the role of the hypertrophied siphonal
epidermis. Biol. Bull. Mar. Biol. Lab. Woods Hole 141: 222234.
Fankboner PV, Reid RGB (1981) Mass expulsion of zooxanthellae by heat-stressed corals: A source
of food for giant clams? Experientia 37: 251252.
Farmer C (1997) Did lungs and the intercardiac shunt evolve to oxygenate the heart in
vertebrates? Paleobiology 23: 358372.
Fenchel TL, Riedl RJ (1971) The sulfide system: A new biotic community underneath the oxidized
layer of marine sand bottoms. Mar. Biol. 7: 255268.
Fisher RA (1930) The Genetical Theory of Natural Selection. Oxford: Clarendon.
Fitch WM, Ayala FJ, eds. (1995) Tempo and Mode in Evolution: Genetics and Paleontology 50
Years after Simpson. Washington: National Academy Press.
Fitt WK (1985) The effect of different strains of the zooxanthellae Symbiodinium microadriaticum
on the growth and survival of their coelenterate and molluscan hosts. Proceedings of the
International Congress on Coral Reefs 6: 131136.
Flamm WG, Walker MB, McCallum M (1969) Some properties of the single strands isolated from
the DNA of the nuclear satellite of the mouse (Mus musculus). J. Mol. Biol. 40: 320443.
Fleming A, Allison VC (1922) Observations on a bacteriolytic substance (lysozyme) found in

secretions and tissues. British J. Exp. Pathology 3: 252260.
Fondon JW III, Garner HR (2004) Molecular origins of rapid and continuous morphological
evolution. Proc. Natl. Acad. Sci. 101: 1805818063.
Foster JB (2000) Marxs Ecology. New York: Monthly Review Press.
Frank AB (1877) Ueber der biologischen Verhltnisse des thallus eineger Krustenflechten. Beitrage
zur Biologie der Pflanzen 195: 123200.
Frankov S (1987) Contribution of the concepts of constraints and developmental plasticity to

the study of behavioral ontogeny and phylogeny. In Behaviour as One of the Main Factors of
Evolution, ed. Leonovicov V, Novk V. Prague: Czechoslovak Academy of Sciences.
ffrench-Constant RH, Bowen DJ (2000) Novel insecticidal toxins from nematode-symbiotic

bacteria. Cell. Mol. Life Sci. 57: 828833.
Frey E, Sues HD, Munk W (1997) Gliding mechanism in the Late Permian reptile Coelurosauravus.
Science 275: 14501452.
Fruton J (1999) Proteins, Enzymes and Genes: The Interplay of Chemistry and Biology. New
Haven: Yale University Press.
Fryer G, Iles TD (1972) The Cichlid Fishes of the Great Lakes of Africa: Their Biology and
Evolution. Edinburgh: Oliver and Boyd.
Fukatsu T, Ishikawa H (1992) Occurrence of chaperonin 60 and chaperonin 10 in primary and

secondary bacterial symbionts of aphids: Implications for the evolution of an endosymbiotic
system in aphids. J. Mol. Evol. 36: 568577.
Bibliography 477
Futuyama DJ (1998) Evolutionary Biology, third edition. Sunderland MA: Sinauer.
Galton F (1869) Hereditary Genius, and Inquiry into Its Laws. London: Macmillan.
Gnti T (1975) Organization of chemical reactions into dividing and metabolizing units: The
chemotons. BioSystems 7: 189195.
Garstang W (1928) The origin and evolution of larval forms. Proceedings of the British
Association for the Advancement of Science D: 123.
Garstang W (1951) Larval Forms and Other Zoological Verses. Oxford: Blackwell.
Gehring WJ (1998) Master Control Genes in Development and Evolution: The Homeobox Story.
New Haven: Yale University Press.
Geoffroy de St H (1818) Philosophie anatomique, volume 1. Paris.
Geoffroy de St H (1822) Philosophie anatomique, volume 2. Paris.
Geoffroy de St H (1833) Mmoire sur le degr dinfluence du monde ambiant pour modifier les
formes animals: Question intressant lorigine des espces tlsauriennes et successivement celle
des animaux de lpoque actuelle. Mmoires de lAcadmie des Sciences 12: 6392.
Geoffroy I de St H (18321836) lHistoire gnerale et particulire des anomalies dorganisation

chez lhomme et les animaux (Trait de tratologie).
Gerard RW (1942) Higher levels of integration. In Biological Symposia VIII, ed. Redfield R.
Lancaster.
Gerhart J, Kirschner M (1997) Cells, Embryos, and Evolution. Oxford: Blackwell Science.
Ghiselin MT (1969) The Triumph of the Darwinian Method. Berkeley: University of California
Press.
Ghiselin MT (1974) A radical solution to the species problem. Systematic Zoology 23: 53644.
Gilbert LI, Tata JR, eds. (1996) Metamorphosis: Postembryonic Reprogramming of Gene
Expression in Amphibian and Insect Cells. Academic Press.
Gilbert SF (1994) Developmental Biology, fourth edition. Sunderland MA: Sinauer.
Gilbert W (1991). A vision of the grail. In The Code of Codes, ed. Kevles D, Hood L. Cambridge:
Gillespie J (1991) The Causes of Molecular Evolution. Oxford: Oxford University Press.
Gleick J (1987) Chaos: Making a New Science. New York: Penguin.
Goebel W, Gross R (2001) Intracellular survival strategies of mutualistic and parasitic prokaryotes.
Trends in Microbiology 9: 267273.
Goldschmidt RB (1940) The Material Basis of Evolution. New Haven: Yale University Press.
Goldschmidt RB (1960) In and Out of the Ivory Tower. Seattle: University of Washington Press.
Goodman M (1981) Decoding the pattern of protein evolution. Prog. Biophys. Mol. Biol. 38:
105164.
478 Bibliography
Goodrich ES (1913) Metameric segmentation and homology. Quart. J. Micr. Sci. 59: 227248.
Goodwin BC (1989) Evolution and the generative order. In Theoretical Biology, ed. Goodwin B,
Saunders P. Edinburgh: Edinburgh University Press.
Goodwin BC (1991) Development. London: Hodder and Stoughton and Open University.
Goodwin BC (1994) How the Leopard Changed its Spots: The Evolution of Complexity. New
York: Simon and Schuster.
Goodwin BC (1995) Biology is just a dance. In The Third Culture, ed. Brockman J. New York:
Simon and Schuster.
Goodwin BC, Saunders PT, eds. (1989) Theoretical Biology: Epigenetic and Evolutionary Order
from Complex Systems. Edinburgh: Edinburgh University Press.
Gorces VG (1995) Keeping enhancers under control. Nature 376: 462463.
Gordon DM (1999) Ants at Work. New York: Free Press.
Gordon DM, Goodwin BC, Trainor LH (1992) A parallel distributed model of ant colony
behaviour. J. Theor. Biol. 156: 293307.
Gottlieb G (1976) The roles of experience in the development of behavior and the nervous
system. In Neural and Behavioral Specificity, ed. Gottlieb G. Academic Press.
Gottlieb G (1987) The developmental basis of evolutionary change. J. Comp. Psych. 101:
262271.
Gottlieb G (1992) Individual Development and Evolution. Oxford: Oxford University Press.
Goudge TA (1961) The Ascent of Life: A Philosophical Study of the Theory of Evolution. Toronto:
University of Toronto Press.
Gould SJ (1974) The evolutionary significance of bizarre structures: Antler size and skull size in
the Irish elk, Megaloceros giganteus. Evolution 28: 191220.
Gould SJ (1977a) Ontogeny and Phylogeny. Cambridge: Belknap.
Gould SJ (1977b) Ever Since Darwin: Reflections in Natural History. New York: Norton.
Gould SJ (1980a) The pandas thumb. In The Pandas Thumb. New York: Norton.
Gould SJ (1980b) Is a new and general theory of evolution emerging? Paleobiology 6: 119130.
Gould SJ (1983a) Helpful monsters. In Hens Teeth and Horses Toes. New York: Norton.
Gould SJ (1983b) Quaggas, coiled oysters, and flimsy facts. In Hens Teeth and Horses Toes. New
York: Norton.
Gould SJ (1983c) Hens teeth and horses toes. In Hens Teeth and Horses Toes. New York: Norton.
Gould SJ (1989). Wonderful Life: The Burgess Shale and the Nature of History. New York: Norton.
Gould SJ (1991) The disparity of the Burgess Shale arthropod fauna and the limits to cladistic
analysis: Why we must strive to quantify morphospace. Paleobiology 8: 415.
Gould SJ (1994) The evolution of life on the earth. Sci. Am. 271 October: 8591.
Bibliography 479
Gould SJ (1995) The Macroevolutionary reconstruction of Darwinism. In Tempo and Mode in

Evolution, ed. Fitch W, Ayala F. Washington: National Academy Press.
Gould SJ (1997) Darwinian fundamentalism. New York Review of Books, June 12.
Gould SJ (2002) The Structure of Evolutionary Theory. Cambridge: Belknap.
Gould SJ, Lewontin R (1979) The spandrels of San Marco and the Panglossian paradigm: A
critique of the adaptationist program. Proc. Roy. Soc. B205: 581598.
Gould SJ, Vrba E (1982) Exaptationa missing term in the science of form. Paleobiology 8: 415.
Grady D (1996) Quick-change pathogens gain an evolutionary edge. Science 274: 1081.
Grant PR, Grant BR (1994) Phenotypic and genetic effects of hybridization in Darwins finches.
Grass P-P, ed. (19481975) Trait de zoologie. Paris: Masson.
Grass P-P, ed. (1973) Lvolution du vivant. Paris: Albin Michel.
Grass P-P, ed. (1977) Evolution of Living Organisms. New York: Academic Press.
Graur D, Li WH (2000) Fundamentals of Molecular Evolution, second edition. Sunderland MA:

Sinauer.
Greene JC (1971) Science, Ideology, and World View. Berkeley: University of California Press.
Greene RW (1970) Symbiosis in sacoglossan opisthobranchs: Symbiosis with algal chloroplasts.

Malacologia 10: 357368.
Greenwood PH (1974) The cichlid fishes of Lake Victoria, East Africa: The biology and evolution
of a species flock. Bull. British Mus. Nat. Hist (Zool.) Supplement 6: 1134.
Gregorini O (1986) Evolution, Development and Cancero-genesis. Il Programma Vita Edizione

Minarelli.
Gregory WK (1934) Polyisomerism and anisomerism in cranial and dental evolution among
vertebrates. Proc. Natl. Acad. Sci. 20: 19.
Grehan JR (1984) Evolution by law. Croizats orthogeny and Darwins Laws of Growth.
Tuatara 27: 1419.
Grehan JR, Ainsworth R (1985) Orthogenesis and evolution. Syst. Zool. 34: 174192.
Greider CW (1998) Telomeres and senescence: The history, the experiment, the future. Current
Biology 8: R178R181.
Greksa LP (1996) Evidence of a genetic basis to the enhanced total lung capacities of Andean
Highlanders. Human Biology 68: 119129.
Grmillet D, Chauvin C, Wilson RP, Le Maho Y, Wanless S (2005) Unusual feather structure allows
partial plumage wettability in diving great cormorants Phalacrocorax carbo. Journal of Avian
Biology 36: 5763.
Grmillet D, Wanless S (2000) Fast food dive-in. NREC news release, August 30.
Grene M (1988) Is evolution at a crossroads? Evolutionary Biology 24: 5181.

480 Bibliography
Grimes GW, Aufderheide KJ (1991) Cellular Aspects of Pattern Formation: The Problem of
Assembly. Basel: Karger.
Grunstein M (1992) Histones as regulators of genes. Sci. Am. 267: 6874.
Gustafson R, Reid RGB (1988a) Larval and post-larval morphogenesis in the gutless protobranch
bivalve Solemya reidi (Cryptodonta: Solemyidae). Mar. Biol. 97: 373387.
Gustafson R, Reid RGB (1988b) Association of bacteria with larvae of the gutless protobranch
bivalve Solemya reidi (Cryptodonta: Solemyidae). Mar. Biol. 97: 389401.
Haake W (1895) Gestalten und Vererbung. Leipzig: Veigel.
Haines LR (2002) The Identification and Partial Characterization of Molecules Found within the
Midgut of the Tsetse Fly. MSc Thesis, University of Victoria, B.C.
Haldane JBS (1932) The Causes of Evolution. London: Longman.
Haldane JS (1913) Mechanism, Life and Personality. London: Murray.
Halder AM, Callaerts O, Gehring WJ (1995) Induction of ectopic eyes by targeted expression of
the eyeless gene in Drosophila. Science 267: 17881792.
Hall BK (1978) Developmental and Cellular Skeletal Biology. New York: Academic Press.
Hall BK (1992) Evolutionary Developmental Biology. London: Chapman and Hall.
Hall BK, ed. (1994) Homology. San Diego: Academic Press.
Hall BK (1999a) Evolutionary Developmental Biology, second edition. Dordrecht: Kluwer.
Hall BK (1999b) The Neural Crest in Development and Evolution. New York: Springer-Verlag.
Hall BK (2000) Balfour, Garstang, de Beer: The first century of evolutionary embryology. Amer.
Zool. 40: 718728.
Hall BK (2001) Organic selection: Proximate environmental effects on the evolution of

morphology and behaviour. Biology and Philosophy 16: 215237.
Hall BK, Pearson R, Mller GB, eds. (2003) Environment, Development and Evolution: Toward a
Synthesis. Cambridge: MIT Press.
Hall TS (1969) Ideas of Life and Matter. Chicago: University of Chicago Press.
Hamburger V (1980) Embryology and the modern synthesis in evolutionary theory. In The
Haraway DJ (1976) Crystals, Fabrics and Fields: Metaphors of Organicism in Twentieth Century
Developmental Biology. New Haven: Yale University Press.
Hardy AC (1954) Escape from specialization. In Evolution as a Process, ed. Huxley J, Hardy A,
Ford E. London: Allen and Unwin.
Hardy AC (1965) The Living Stream. London: Collins.
Hawkes N (1997) Is science nearing the final frontier? Review of John Horgans The End of
Science. Times (London), May 5.
Bibliography 481
Heddi A, Charles H, Khatchadourian C (2001) Intracellular bacterial symbiosis in the genus

Sitophilus: The biological individual concept revisited. Res. Microbiol. 152: 431457.
Hedges SB, Parker PH, Sibley CG, Kumar S (1996) Continental breakup and the ordinal diversifi-
cation of birds and mammals. Nature 381: 226229.
Henderson LJ (1917) The Order of Nature. Cambridge: Harvard University Press.
Herring SW (1993) Formation of the vertebrate face: Epigenetic and functional influences.
American Zoologist 33: 472483.
Heslop-Harrison J (1983) Chromosomes, cladism and the new evolutionary debate. In Kew
Chromosomal Conference II, ed. Brandham P, Bennett M. London: Allen and Unwin.
Himmelfarb G (1959) Darwin and the Darwinian Revolution. Garden City NY: Doubleday.
His W (1874) ber unsere Krperform. Leipzig: Vogel.
Ho M-W (1984) Environment and heredity in development and evolution. In Beyond Neo-
Darwinism, ed. Ho M-W, Saunders P. London: Academic Press.
Ho M-W, Saunders PT (1982) Adaptation and natural selection: Mechanisms and teleology. In
Towards a Liberatory Biology, ed. Rose S. London: Allison and Busby.
Hochachka P (1973) Comparative intermediary metabolism. In Comparative Animal Physiology,

third edition, ed. Prosser C. Saunders.
Holland JH (1998) Emergence. From Chaos to Order. Reading MA: Addison-Wesley.
Holliday R (1993) Epigenetic inheritance based on DNA methylation. In DNA Methylation, ed.
Jost J, Saluz H. Birkhauser.
Holliday R (1994). Epigenetics: An overview. Developmental Genetics 15: 453457.
Honderich T, ed. (1995) The Oxford Companion to Philosophy. Oxford: Oxford University Press.
Hooper LV, Wong MH, Thalin A, Hasson L, Falk PG, Gordon JI (2001) Molecular analysis of
commensal host-microbial relationships in the intestine. Science 291: 881884.
Horder TJ (1994) Partial truths: A review of the use of concepts in evolutionary science. In Models
in Phylogeny Reconstruction, ed. Scotland R, Siebert D, Williams D. Oxford: Clarendon.
Horgan J (1996) The End of Science. New York: Addison-Wesley (Broadway Books, 1997).
Horowitz NH (1945) Evolution of biochemical syntheses. Proc. Nat. Acad. Sci. 31: 153157.
Hovasse R (1950) Adaptation et volution. Paris: Hermann.
Hughes AJ, Lambert DM (1984) Structuralism, functionalism, and ways of seeing. J. Theor. Biol.
111: 787800.
Hume D (1748) Philosophical Essays Concerning Human Understanding. London.
Humphrey N. 1995. The thick moment. In The Third Culture, ed. Brockman J. New York: Simon
and Schuster.
Hurst LD (1992) Intragenomic conflict as an evolutionary force. Proc. Roy. Soc. B248: 135140.
Hurst LD, Randerson JP (2002) Parasitic sex puppeteers. Sci. Am. 287, April: 5661.
482 Bibliography
Hutton FW (1899) Darwinism and Lamarckism. London: Duckworth.
Huxley J (1942) Evolution: The Modern Synthesis. London: Allen & Unwin. Second edition,
1962; third edition, 1974.
Huxley J (1948) Man in the Modern World. New York: Harper and Row, Mentor.
Huxley TH (1864) Criticisms on The Origin of Species. Nat. Hist. Rev. New Series 4: 2536.
Huxley TH (1882) The Coming of Age of the Origin of Species. Proc. Roy. Inst. 9: 361368.
Huxley TH (1894) Owens position in the history of anatomical science: Appendix to volume 3.
In R. Owen, The Life of Richard Owen. London: Murray.
Imms AD (1957) A General Textbook of Entomology, ninth edition. London: Methuen.
Jablonka E, Lamb MJ (1995) Epigenetic Inheritance and Evolution: The Lamarckian Dimension.
Oxford: Oxford University Press.
Jablonka E, Lamb MJ (2005) Evolution in Four Dimensions: Genetic, Epigenetic, Behavioral and
Symbiolic Variation in the History of Life. Cambridge: MIT Press.
Jablonski D (1986) Larval ecology and macroevolution in marine invertebrates. Bull. Marine Sci.
39: 565587.
Jacob F, Monod J (1961) Genetic regulatory mechanisms in the synthesis of proteins. J. Mol. Biol.
3: 31856.
Jegalian K, Page DC (1998) A proposed path by which genes common to mammalian X and Y
chromosomes evolve to become X inactivated. Nature 394: 776780.
Jegalian K, Lahn BR (2001) Why the Y is so weird. Sci. Am. 284, February: 5661.
Jennings HS (1927) Diverse doctrines of evolution, their relation to the practice of science and of
life. Science 65: 1925.
Jiminez G, Ford AM, Enver T, Boronat A (1993) Multiple changes in chromatin structure precede
the transcriptional activation of the human growth hormone locus in placental cells. Molecular
and Cellular Endocrinology 96: 5360.
Johnson PE (1993) Darwin on Trial. Downers Grove IN: InterVarsity.
Johnston N (2004) Seeds of a micro revolution. The-scientist.com.
Jones FW (1943) Habit and Heritage. London: Routledge.
Jones S (1995) Why is there so much genetic diversity? In The Third Culture, ed. Brockman J.
New York: Simon and Schuster.
Kane J (1995) Savages. Vancouver: Douglas and Stewart.
Kauffman SA (1989) Origins of order in evolution: Self-organization and selection. In Theoretical

Biology, ed. Goodwin B, Saunders P. Edinburgh: Edinburgh University Press.
Kauffman SA (1991) Antichaos and adaptation. Sci. Am. 265, August: 7884.
Kauffman SA (1993) Origins of Order: Self-Organization and Selection in Evolution. New York:
Oxford University Press.
Bibliography 483
Kauffman SA (1995) At Home in the Universe. New York: Oxford University Press.
Kayzer W (1996) A Glorious Accident. TV Matters.
Keller EF (1983) A Feeling for the Organism. San Francisco: Freeman.
Keller EF (1995) Refiguring Life: Metaphors of Twentieth-Century Biology. New York: Columbia
University Press.
Keller EF (2002) Making Sense of Life. Cambridge: Harvard University Press.
Kellner RL (2002) Molecular identification of an endosymbiotic bacterium associated with

pederin biosynthesis in Paeder sabaeus (Coleoptera: Staphylinidae). Insect Biochem. Mol. Biol. 32:
389395.
Kennison JA (1993) Transcriptional activation of Drosophila homeotic genes from distant

regulatory sites. Trends Genet. 9: 7579.
Kim J (1999) Making sense of emergence. Phil. Studies 95: 336.
Kimura M (1960) Optimum mutation rate and degree of dominance as determined by the
principle of minimum genetic load. J. Genetics 57: 2134.
King DG (1994) Triple repeat DNA as a highly mutable regulatory mechanism. Science 263:
595596.
King DG, Soller M, Kashi Y (1994) Evolutionary tuning knobs. Endeavour 21: 3640.
King RC, Stansfield WD (1984) A Dictionary of Genetics, third edition. Oxford: Oxford University
Press.
Kingsolver JG, Hoekstra JM, Berrigan D, Vignieri SN, Hill CE, Hoang A, Gibert P, Beerli P (2001)
The strength of phenotypic selection in natural populations. Am. Nat. 157: 245261.
Kirschner MW, Gerhart JC (2005) The Plausibility of Life: Resolving Darwins Dilemma. New
Klenk H-P et al. (1997) The complete genome sequence of the hyperthermophilic, sulphate-
reducing archaeon Archaeoglobus fulgidus. Nature 390: 364370.
Kobayashi M, Inaba H (2000) Photon statistics and correlation analysis of ultraweak light
originating from living organisms. Applied Optics 39: 183.
Koch AL (1993) Genetic response of microbes to extreme challenges. J. Theor. Biol. 160: 121.
Koch C, Laurent G (1999) Complexity and the nervous system. Science 284: 96101.
Koestler A (1964) The Act of Creation. London: Hutchinson.
Koestler A (1967) The Ghost in the Machine. London: Hutchinson.
Koestler A, Smythies JR (1969) Beyond Reductionism: New Perspectives in the Life Sciences.
London: Hutchinson.
Kolesnikova LA (1987) Evolution of the pineal gland and its changes during selection of silver
foxes for domestic behaviour. In Behaviour as One of the Main Factors of Evolution, ed.
Leonovicov V, Novk V. Prague: Czechoslovak Academy of Sciences.
484 Bibliography
Kollar EJ, Fisher C (1980) Tooth induction in chick epithelium: Expression of quiescent genes for
enamel synthesis. Science 207: 993995.
Klliker RA von (1864) Ueber die Darwinsche Schopfungstheorie ein Vortrag. Zeit. Wiss. Zool. 14.
Kolnicki R (1999) Karyotypic fission theory applied: Kinetochore reproduction and lemur
evolution. Symbiosis 26: 123141.
Kolnicki R (2000) Kinetochore reproduction in animal evolution: Call biological explanation of

karyotypic fission theory. Proc. Natl. Acad. Sci. 97: 94939497.
Kornegay JR, Schilling JW, Wilson AC (1994) Molecular adaptation of a leaf eating bird: Stomach
lysozyme of the hoatzin. Mol. Biol. Evol. 11: 921928.
Krebs AI, Houston JI (1989) Optimization in ecology. In Ecological Concepts, ed. Cherrett M.
Blackwell Scientific.
Kuhn TS (1962) The Structure of Scientific Revolutions. Chicago: University of Chicago Press
(2nd Edition 1970).
Kuhn TS (2000) The Road since Structure, ed. Conant J, Haugeland J. Chicago: University of
Chicago Press.
Kukalova-Peck J (1983) Origin of the insect wing and wing articulation from the arthropodan leg.
Can. J. Zool. 61: 1618165.
Lachmansingh E, Rollo CD (1994) Evidence of a trade-off between growth and behavioural

activity in giant supermice genetically engineered with extra growth hormone genes. Can. J.
Zool. 72: 21582168.
Lahn BR, Page DC (1997) Functional coherence of the human Y chromosome. Science 278:
675680.
Lahn BR, Page DC (1999) Four evolutionary strata on the human X chromosome. Science 286:
964967.
Lamarck J-B (1809) La philosophie zoologique. Paris. Reissued in Naturalis Classica series
(Wheldon and Wesley).
Lamarck J-B (181522) LHistoire naturelle des animaux sans vertebres. Paris.
Langton CB (1992) Adaptation to the edge of chaos. In Artificial Life II, ed. Langton C, Farmer J,
Rasmussen A, Taylor C. Reading MA: Addison-Wesley.
Larsen EW (2004) A view of phenotypic plasticity from molecules to morphogenesis. In Environ-

ment, Development and Evolution, ed. Hall B, Pearson R, Mller G. Cambridge: MIT Press.
Laudet V (1997) Evolution of the nuclear receptor superfamily: Early diversification from an
ancestral orphan receptor. J. Mol. Endocrinology 19: 207226.
Laudet V, Hanni C, Coll J, Catzeflis F, Stehelin D (1992) Evolution of the nuclear receptor gene
superfamily. EMBO J. 11: 10031013.
Law MS, Change KW, Fung TK, Chan YH, Yu KL, Chan KM (1996) Isolation and characterization
of two distinct growth hormone cDNAs from the goldfish, Carassius uratus. Archives of
Biochemistry and Biophysics 33: 1923.
Bibliography 485
Lederberg J (1951) Genetic studies in bacteria. In Genetics in the Twentieth Century, ed. Dunn L.
New York: Macmillan.
Lee S-H, Fu KK, Hui JN, Richman JM (2001) Noggin and retinoic acid transform the identity of
avian facial prominences. Nature 414: 909912.
Le Livre CS (1978) Participation of neural crest-derived cells in the genesis of the skull in birds.
J. Embryol. Exp. Morph. 47: 1637.
Le Maho Y (1977) The emperor penguin: A strategy to live and breed in the cold. Am. Sci. 65:
680696.
Leroi AM (1998) The burden of the bauplan. Trends in Ecology and Evolution 13: 8283.
Levinton JS (1992) The big-bang of animal evolution. Sci. Am. 267, November: 8491.
Levit G, Hossfeld U (2006) The forgotten old-fashioned synthesis: The evolutionary theory of
Ludwig H. Plate (18621937). Internationale Zeitschrift fr Geschichte und Ethik der
Naturwissenschaften, Technik und Medizin 14: 925.
Lewes GH (1874, 1875). Problems of Life and Mind. London: Trubner.
Lewin B (1997) Genes VI. New York: Oxford University Press.
Lewin R (1988) A heresy in evolutionary biology. Research News, September 16: 1431.
Lewis JA, Davide JP, Melera PW (1982) Selective amplification of polymorphic dihydrofolate
reductase gene loci in Chinese hamster lung cells. Proc. Natl. Acad. Sci. 79: 69616965.
Lewontin R (2000) The Triple Helix: Gene, Organism, and Environment. Cambridge: Harvard
University Press.
Li W-H, Graur D (1991). Fundamentals of Molecular Evolution. Sunderland MA: Sinauer.
Li W-H, Gu Z, Wang H, Nekrutenko A (2001) Evolutionary analyses of the human genome.

Nature 409: 847849.
Lima-de-Faria A (1988) Evolution without Selection: Form and Function by Autoevolution.

Amsterdam: Elsevier.
Lin Y, Waldman AS (2001) Capture of DNA sequences at double-strand breaks in mammalian

chromosomes. Genetics 158: 16651674.
Lincoln R, Boxshall G, Clark P (1998) A Dictionary of Ecology, Evolution and Systematics, second
edition. Oxford: Oxford University Press.
Linde A (1994) The self-reproducing inflationary universe. Sci. Am. 271, November: 4855.
Little KC, Chartrand P (2004) Genomic DNA is captured and amplified during double-strand
break (DSB) repair in human cells. Oncogene 23: 41664172.
Livant W (1988) The rise of reproduction: Ten propositions. In Evolution of Social Behavior and
Integrative Levels, ed. Greenberg G, Tobach E. New Jersey: Lawrence Erlbaum Assoc.
Livant W (1998) Bill Livants cure for baldness. Science and Society 62: 471474.
Lloyd RE (1914) What Is Adaptation? London: Longman.

486 Bibliography
Logsdon JF, Doolittle RF (1997) Origin of antifreeze protein genes: A cool tale in molecular
evolution. Proc. Natl. Acad. Sci. 94: 34853487.
Long CA (1976) Evolution of mammalian cheek pouches and a possibly discontinuous origin of
a higher taxon (Geomyoidea). Am. Nat. 110: 10931111.
Lotka AJ (1922) Contribution to the energetics of evolution. Proc. Natl. Acad. Sci. 8: 147162.
Lovejoy AO (1927) The meaning of emergence and its modes. J. Philos. Studies 2: 167189.
Lovejoy AO (1936) The Great Chain of Being. Cambridge: Harvard University Press.
Lovelock JE (1979) Gaia: A New Look at Life on Earth. Oxford: Oxford University Press.
Lovelock JE (1988) The Ages of Gaia. New York: Norton.
Lvtrup S (1974) Epigenetics. New York: Wiley.
Lvtrup S (1975) Letter. Syst. Zool. 24: 507511.
Lvtrup S (1983) Reduction and emergence. Rivista di BiologiaBiology Forum 76: 437461.
Lvtrup S (1992) Human evolution and epigenesis. Human Evolution 7: 2531.
Lwoff A (1944) Lvolution physiologique. Paris: Hennann.
Lyell C (183033) Principles of Geology. London: John Murray.
Macbeth N (1971) Darwin Retried. New York: Dell.
MacFadden BJ (1986) Fossil horses from Eohippus to Equus: Scaling, Copes law, and the
evolution of body size. Paleobiology 12: 355369.
Mackie GO (1999) Coelenterate organs. Mar. Fresh. Behav. Physiol. 32: 113127.
Magee PT (1997) Which came first, the hypha or the yeast? Science 277: 5253.
Magnum CP, Towle D (1977) Physiological adaptation to unstable environments. Am. Sci. 65:
6775.
Marcotrigniano M (1999) Chimeras and variegation: Patterns of deceit. Horticultural Science 32:
773784.
Maret TJ, Collins JP (1997) Ecological origin of morphological diversity: A study of alternative
trophic phenotypes in larval salamanders. Evolution 51: 898905.
Margulis L (1970) Origin of Eukaryotic Cells. New Haven: Yale University Press.
Margulis L (1981) Symbiosis in Cell Evolution: Life and Its Environment in the Early Earth. San
Francisco: Freeman.
Margulis L (1998) Symbiotic Planet: A New View of Evolution. New York: Basic Books.
Margulis L, Sagan D (2002) Acquiring Genomes: A Theory of the Origins of Species. New York:
Basic Books.
Martin MO, Benford G (1996) A Darker Geometry. New York: Baen Books.
Martin WF, Muller M (1998) The hydrogen hypothesis for the first eukaryote. Nature 392: 3741.
Bibliography 487
Maser C, Trappe JM, Nusbaum RA (1978) Fungal-small mammal interrelationships with emphasis
on Oregon coniferous forests. Ecology 59: 799809.
Matsuda R (1982) The evolutionary process in talitrid amphipods and salamanders in changing
environments with a discussion of genetic assimilation and some other evolutionary
comments. Can. J. Zool. 60: 73349.
Matsuda R (1987) Animal Evolution in Changing Environments with Special Reference to

Abnormal Metamorphosis. New York: Wiley.
Maudlin I, Wellburn SC, Mehlitz D (1990) The relationship between rickettsia-like organisms and
trypanosome infections in natural populations of tsetse in Liberia. Tropical Medicine and
Parasitology 41: 265267.
Maynard Smith J (1978) The Evolution of Sex. Cambridge: Cambridge University Press.
Maynard Smith J (1988) Evolutionary progress and levels of selection. In Evolutionary Progress,
ed. Nitecki H. Chicago: University of Chicago Press.
Maynard Smith J, Szathmry E (1995) The Major Transitions of Evolution. Oxford: Oxford
University Press.
Mayr E (1942) Systematics and the Origin of Species. New York: Columbia University Press.
Mayr E (1954) Change of genetic environment and evolution. In Evolution as a Process, ed.
Huxley J, Hardy A, Ford E. London: Allen and Unwin.
Mayr E (1959) Where are we? Cold Spring Harbor Symp. Quant. Biol. 24: 114.
Mayr E (1960) The emergence of evolutionary novelties. In Evolution after Darwin, volume 1, ed.
Tax S. Chicago: University of Chicago Press.
Mayr E (1961) Cause and effect in biology. Science 134: 15011506.
Mayr E (1963) Animal Species and Evolution. Cambridge: Harvard University Press.
Mayr E (1972) The nature of the Darwinian revolution. Science 176: 981987.
Mayr E (1980) Prologue: Some thoughts on the history of the evolutionary synthesis. In The
Mayr E (1982) The Growth of Biological Thought. Cambridge: Belknap.
Mayr E (1991) One Long Argument: Charles Darwin and the Genesis of Modern Evolutionary
Thought. Cambridge: Harvard University Press.
McClintock B (1951) Chromosome organization and genic expression. Cold Spring Harbor Symp.
Quant. Biol. 16: 1347.
McClintock B (1956) Controlling elements and the gene. Cold Spring Harbor Symp. Quant. Biol.
21: 215249.
McClintock B (1978) Mechanisms that rapidly reorganize the genome. In Stadler Symposium 10,
ed. Reder G. New York: Columbia University Press.
McClintock B (1980) Modified gene expressions induced by transposable elements. In

Mobilization and Reassembly of Genetic Information, ed. Scott W. New York: Academic Press.
488 Bibliography
McDougall W (1927) Modern Materialism and Emergent Evolution. New York: Van Nostrand.
McLaren A, Michie D (1958) An effect of the uterine environment upon skeletal morphology in
the mouse. Nature 181: 11471148
McMenamin M (1998) The Garden of Ediacara. New York: Columbia University Press.
McMillan HJ, Wynne-Edwards KE (1998) Evolutionary change in the endocrinology of behavioral

receptivity: Divergent roles for progesterone and prolactin within the genus Phodopus. Biology of
Reproduction 59: 3038.
McMillan HJ, Wynne-Edwards KE (1999) Divergent reproductive endocrinology of the estrous

cycle and pregnancy in dwarf hamsters (Phodopus). Comp. Biochem. Physiol. A 124: 5367.
McNeil M (1987) Under the Banner of Science. Erasmus Darwin and His Age. Manchester:
Manchester University Press.
Medawar P (1951) Problems of adaptation. New Biol. 11: 1015.
Meir E, Dassow B von, Munro E, Odell GM (2002) Robustness, flexibility, and the role of lateral
inhibition in the neurogenic network. Current Biology 12: 778786.
Menge BA, Berlow, EL, Blanchette CA, Navarrete SA, Yamada SB (1994)The keystone species
concept: Variation in interaction strength in a rocky intertidal habitat. Ecological Monographs
64: 249286.
Metz CW (1947) Duplication of chromosome parts as a factor in evolution. Am. Nat. 81: 81103.
Meyer-Abich A (1964) The Historico-Philosophical Background of Modern Evolution Biology.

Leiden: Brill.
Mill J S (1843) A System of Logic, Ratiocinative and Inductive. In The Collected Works of John
Stuart Mill, volumes 7 and 8 (Toronto: University of Toronto Press, 1973).
Miller J, Fraser SE, McClay D (1995) Dynamics of thin filipodia during sea urchin gastrulation.
Development 121: 25012511.
Milne Edwards H (1834) lHistoire naturelle des Crustacs, comprenant lanatomie, la physiologie
et la classification de ces animaux. Paris.
Milne Edwards H (1834) lmens de zoologie, ou leons sur lanatomie, la physiologie, la classi-
fication et les moeurs des animaux. Paris.
Milne Edwards H (1841) Outlines of Anatomy and Physiology. Boston.
Mitchell SD (2003) Biological Complexity and Integrative Pluralism. Cambridge: Cambridge

University Press.
Mivart SGJ (1871) On the Genesis of Species. London: Macmillan.
Monk M (1995) Epigenetic programming of differential gene expression in development and

evolution. Developmental Genetics 17: 188197.
Monod J (1971) Chance and Necessity. New York: Knopf.
Morgan CL (1891) Animal Life and Intelligence. London: Arnold.

Bibliography 489
Morgan CL (1896) Habit and Instinct. London: Arnold.
Morgan CL (1923) Emergent Evolution. London: Williams & Norgate.
Morgan CL (1933) The Emergence of Novelty. London: Williams & Norgate.
Morgan TH (1903) Evolution and Adaptation. London: Macmillan.
Morgan WF, Bodycote J. Fero ML, Hahn PJ, Kapp LN, Pantelias GE, Painter RB (1986) A
cytogenetic investigation of DNA replication after hydroxyurea treatment: Implications for gene
amplification. Chromosoma 93: 191196.
Morin S, Ghanim M, Sobol I, Czosnek H (2000) The GroEL protein of the whitefly Bemisia tabaci
interacts with the coat protein of transmissible and nontransmissible begoviruses in the yeast
two-hybrid system. Virology 276: 404416.
Morwood MJ, Soejono RP, Roberts RG, Sutikna T, Turney CSM, Westaway KE, Rink WJ, Ahzo J-X,
van den Bergh GD, Rokus AD, Hobbs DR, Moore MW, Bird MI, Fifield LK (2004) Archaeology and
age of a new hominin from Flores in eastern Indonesia. Nature 431: 10871091.
Moxon RE, Wills C (1999) DNA microsatellites: Agents of evolution? Sci. Am. 280, January:
9499.
Muir A, Lever A, Moffett A (2004) Expression and functions of human endogenous retroviruses
in the placenta: An update. Placenta 25: S16S25.
Muir W, Howard R (1999) Possible ecological risks of transgenic organism release when
transgenes affect mating success: Sexual selection and the Trojan gene hypothesis. Proc. Natl.
Acad. Sci. 96: 1385313856.
Mller GB (1991) Developmental mechanisms at the origin of morphological novelty: A side-

effect hypothesis. In Evolutionary Innovations, ed. Nitecki M. Chicago: University of Chicago
Press.
Mller GB, Newman SA (2003) Origination of Organismal Form: Beyond the Gene in
Development and Evolutionary Biology. Cambridge: MIT Press.
Mller GB, Streicher J (1989) Ontogeny of the syndesmosis tibiofibularis and the evolution of the
bird hindlimb: A caenogenetic feature triggers phenotypic novelty. Anatomy and Embryology
179: 327339.
Mller GB, Wagner GP (1991) Novelty in evolution: Restructuring the concept. Ann. Rev. Ecology
and Systematics 22: 229256.
Mller GB, Wagner GP (1996) Homology, Hox genes, and developmental integration. Am. Zool.
36: 413.
Muller HJ (1930) Types of visible variations induced by X-rays in Drosophila. J. Genet. 22:
299314.
Murphy JJ (1869) Habit and Intelligence. London: Macmillan.
Murray MA, Schubinger ML, Palka J (1981) Preferred axon paths in the wing of Drosophila. Soc.
Neurosci. Abstracts 7: 347356.
490 Bibliography
Nagel T (1978) Mortal Questions. Cambridge: Cambridge University Press.
Ngeli C von (1884) Mechanisch-Physiologische Theorie der Abstammungslehre. Leipzig:

Oldenbourg.
Nash MJ (1995) When life exploded. Time 146, no. 23: 3846.
Nelson G (1970) Outline of a theory of comparative biology. Syst. Zool. 19: 373384.
Newcombe RD, Campbell PM, Ollis DL, Cheah E, Russell RJ, Oakshott JG (1997) A single amino
acid substitution converts a carboxylesterase to an organophosphorus hydrolase and confers
insecticide resistance on a blowfly. Proc. Natl. Acad. Sci. 94: 74647468.
Newman SA (1993) Is segmentation generic? Bioessays 15: 277283.
Newman SA, Mller GB (2000) Epigenetic mechanisms of character origination. J. Exptl. Zool.
(Mol. Dev. Evol.) 288: 304317.
Nicolis G, Prigogine I (1977) Self-Organization in Non-Equilibrium Systems. New York: Wiley.
Nielsen C (1995) Animal Evolution: Interrelationships of the Living Phyla. Oxford: Oxford
University Press.
Niklas KJ (1997) The Evolutionary Biology of Plants. Chicago: University of Chicago Press.
Nitecki MH, ed. (1988) Evolutionary Progress. Chicago: University of Chicago Press.
Nitecki MH, ed. (1990) Evolutionary Innovations. Chicago: University of Chicago Press.
Novick A, Weiner M (1957) Enzyme induction as an all-or-none phenomenon. Proc. Natl. Acad.
Sci. 43: 553566.
Novick RP (1980) Plastids. Sci. Am. 243, December: 103124.
Novick RP (1998) Contrasting lifestyles of rolling-circle phages and plasmids. Trends in

Biochemical Sciences 23: 434438.
Nowak R (1994) Mining treasures from junk DNA. Science 263: 608610.
Nsslein-Volhard C (1996) Gradients that organize embryo development. Sci. Am. 273, August:
5461.
Nsslein-Volhard C, Wieschaus E (1980) Mutations affecting segment number and polarity in

Drosophila. Nature 287: 795799.
Ohno S (1970) Evolution by Gene Duplication. Berlin: Springer.
Oldroyd DR (1980) Darwinian Impacts: An Introduction to the Darwinian Revolution. Atlantic

Highlands NJ: Humanities Press.
Oparin AI (1938) The Origin of Life. New York: Macmillan.
Orgel LE (1994) The origin of life on the earth. Sci. Am. 271, October: 7783.
Osborn HF (1896) A mode of inheritance requiring neither natural selection nor inheritance of
acquired character. Trans. New York Acad. Sci. 15: 141148.
Otte D, Endler JA (1989) Speciation and Its Consequences. Sunderland MA: Sinauer.
Bibliography 491
Owen R (1847) Report on the archetype and homologies of the vertebrate skeleton. Rep. Brit.
Assoc. Adv. Sci. 169340.
Oyama S (1985) The Ontogeny of Information. Second edition: Durham NC: Duke University
Press, 2000.
Oyama S (2000) Evolutions Eye. Durham NC: Duke University Press.
Palka J, Schubinger M, Ellison RL (1983) The polarity of axon growth in the wings of Drosophila
melanogaster. Devel. Biol. 98: 481489.
Palmeirim I, Henrique D, Ish-Horowicz D, Pourquie O (1997) Avian hairy gene expression

identifies a molecular clock linked to vertebrate segmentation and somatogenesis. Cell 91:
639648.
Palmiter RD, Brinster RL, Hammer RE (1982) Dramatic growth of mice from eggs microinjected
with metallothionein-growth hormone fusion genes. Nature 300: 611615.
Parrish JE, Oostra BA, Verkerk AJMH, Richards CS, Reynolds J, Spikes AS, Shaffer LG, Nelson DL
(1994) Isolation of a GCC repeat showing expansion in FRAXF, a fragile site distal to FRAXA and
FRAXE. Nature Genetics 8: 229235.
Paterson HEH (1982) Darwin and the origin of species. South African Journal of Science 78:
272275.
Paterson HEH (1985) The recognition concept of species. In Species and Speciation, ed. Vrba E.
Pretoria: Transvaal Museum.
Pawson T, Scott JD (1997) Signalling through scaffold, anchoring and adaptor proteins. Science
278: 20752080.
Pearson RD (1986) Evolutionary theory, regeneration, and cancer. Med. Hypoth. 19: 714.
Pearson RD (1999) Long-billed European starlings, Sturnus vulgaris. Canadian Field Naturalist 113:
523524.
Pearson RD (2004) The determined embryo: Homeodynamics, hormones and heredity. In

Environment, Development and Evolution, ed. Hall B, Pearson R, Mller G. Cambridge: MIT
Press.
Peirce CS (1898) Reasoning and the Logic of Things. A series of lectures given at Harvard
University. First published in Collected Papers of Charles Sanders Peirce; reissued as Reasoning
and the Logic of Things (Cambridge: Harvard University Press, 1992).
Pelling C (1959) Chromosomal synthesis of ribonucleic acid as shown by the incorporation of

uridine labeled with tritium. Nature 184: 655666.
Pennisi E (1998) How the genome readies itself for evolution. Science 281: 113115.
Pepperberg IM (1998) Talking with Alex: Logic and speech in parrots. Scientific American Presents
(Exploring Intelligence) 9, no. 4: 6065.
Pepperberg IM (1999) The Alex Studies: Cognitive and Communicative Abilities of Grey Parrots.
Cambridge: Harvard University Press.
492 Bibliography
Perkowska E, MacGregor HC, Birnstiel ML (1968) Gene amplification in the oocyte nucleus of
mutant and wild-type Xenopus laevis. Nature 217: 649650.
Perru Q (1997) Le concept dindividualit biologique chez Milne-Edwards. Bull. Hist. Epistm. Sc.
Vie 4: 147172.
Peters RH (1991) A Critique for Ecology. Cambridge: Cambridge University Press.
Pfeffer W (1881) Pflanzenphysiologie.
Piaget J (1968) Structuralism. London: Routledge and Kegan Paul.
Piaget J (1978) Behavior and Evolution. New York: Random House.
Pirkkala L, Nykanen P, Sistonen L (2001) Roles of the heat shock transcription factor in regulation
of the heat shock response and beyond. FASEB J. 15, May: 11181131.
Pirozynski KA, Malloch DW (1975) The origin of land plants: A matter of mycotrophism.
Biosystems 6: 153164.
Plate L (1913) Selektionsprinzip und Probleme der Artbildung: Ein handbuch des Darwinismus.
Leipzig: Engelmann.
Polanyi M (1958) Personal Knowledge. London: Routledge and Kegan Paul. Revised edition:
Routledge & Kegan Paul, 1962. Harper Torchbook Edition: 1964.
Polanyi M (1968) Lifes irreducible structure. Science 160: 13081312.
Popper KR (1959) The Logic of Scientific Discovery. New York: Basic Books.
Popper KR (1972) Objective Knowledge, an Evolutionary Approach. Oxford: Oxford University

Press.
Poulton EB (1908) Essays on Evolution 18891907. Oxford: Oxford University Press.
Pray L (2002) Evolutionists present their 1.3% solution. The Scientist 16: 3641.
Pray L (2004) Epigenetics: Genome, meet your environment. The-scientist.com.
Prigogine I, Stengers I (1984) Order out of Chaos. New York: Bantam.
Prody CA, Dreyfuss P, Zamir R, Zakut H, Soreq H (1989) De novo amplification within a silent
human cholinesterase gene in a family subjected to prolonged exposure to organophosphorous
insecticides. Proc. Natl. Acad. Sci. 86: 690694.
Prosser CL (1965) Levels of biological organization and their physiological significance. In Ideas
in Modern Biology, ed. Moore J. New York: Natural History Press.
Provine WB (1971) The Origins of Theoretical Population Genetics. Chicago: University of

Chicago Press.
Provine WB (1978) The role of mathematical population geneticists in the evolutionary synthesis
of the 1930s and 1940s. Studies in History of Biology 2: 167192.
Provine WB (1988) Progress in evolution and meaning in life. In Evolutionary Progress, ed.
Nitecki M. Chicago: University of Chicago Press.
Provine WB (2001) Afterword. In reissued edition of The Origins of Theoretical Population

Genetics. Chicago: University of Chicago Press.
Bibliography 493
Punnett RC (1915) Mimicry in Butterflies. Cambridge: Cambridge University Press.
Radinsky L (1984) Ontogeny and phylogeny in horse skull evolution. Evolution 38: 115.
Raff RA (1996) The Shape of Life. Chicago: University of Chicago Press.
Raff RA, Kaufman TC (1983) Embryos, Genes, and Evolution: The Developmental-Genetic Basis
of Evolutionary Change. New York: Macmillan.
Raff RA, Parr B, Parks A, Wray G (1990) Heterochrony and other mechanisms of radical evolu-
tionary change in early development. In Evolutionary Innovations, ed. Nitecki M. Chicago:
University of Chicago Press.
Raff RA, Wray G (1989) Heterochrony: Developmental mechanisms and evolutionary results. J.
Evol. Biol. 2: 409434.
Raup DM (1972) Taxonomic diversity during the Phanerozoic. Science 177: 10651071.
Raup DM (1986) The Nemesis Affair. New York: Norton.
Raup DM (1991) Extinction: Bad Genes or Bad Luck? New York: Norton.
Rebeck J (1994) Synthetic self-replicating molecules. Sci. Am. 271, July: 4855.
Reid RGB (1985a) Evolutionary Theory: The Unfinished Synthesis. Beckenham: Croom Helm.
Reid RGB (1985b) Unpredicted factors of evolution: The theory of emergence revisited. Rivista di
Biologia 78: 493512.
Reid RGB (1987) The successful monster: Evolution by association. In Towards a New Synthesis
of Evolutionary Biology, ed. Mlikovsky J, Novk V. Prague: Czechoslovak Academy of Sciences.
Reid RGB (1989) The unwhole organism. Amer. Zool. 29: 11331140.
Reid RGB (1990) Evolutionary implications of sulphide-oxidizing symbioses in bivalves. In The

BivalviaProceedings of a Memorial Symposium in Honour of Sir Charles Maurice Yonge,
Edinburgh, 1986, ed. Morton B. Hong Kong: Hong Kong University Press.
Reid RGB (1998) Subclass Protobranchia. In Mollusca: The Southern Synthesis, ed. Beasley P, Ross
G, Wells A. Melbourne: CSIRO.
Reid RGB (2004) Epigenetics and environment: The historical matrix of Matsudas pan-environ-
mentalism. In Environment, Development and Evolution, ed. Hall B, Pearson R, Mller G.
Cambridge: MIT Press.
Reid RGB, Brand D (1986) Sulfide-oxidizing symbioses in lucinaceans: Implications for bivalve
evolution. Veliger 29: 324.
Reimchen TE (2000) Some ecological and evolutionary aspects of bear-salmon interactions in

coastal British Columbia. Can. J. Zool. 78: 448457.
Reimchen TE (2001) Salmon nutrients, nitrogen isotopes and coastal forests. Ecoforestry 16:
1317.
Rendel JM (1979) Canalization and selection. In Quantitative Genetic Variation, ed. Thomson J,
Thoday J. New York: Academic Press.
494 Bibliography
Rensch B (1959) Evolution above the Species Level. London: Methuen.
Riedl R (1978) Order in Living Systems. London: Methuen.
Riley D (1978) Developmental psychology, biology and Marxism. Ideology and Consciousness 4:
7391.
Ring RA (1982) Freezing-tolerant insects with low supercooling points. Comp. Biochem. Physiol.
73A: 605612.
Ring RA, Tesar D (1981) Adaptations to cold in Canadian Arctic insects. Cryobiology 18: 199211.
Ritossa F, Malva C, Boncinelli E, Graziani F, Polito L (1971) The first steps of magnification of
DNA complementary to ribosomal RNA in Drosophila melanogaster. Proc. Natl. Acad. Sci. 68
15801584.
Ritter WE, Bailey EW (1928) The organismal concept, its place in science and bearing on
philosophy. University of California Publications in Zoology 31: 307358.
Robson GC, Richards OW (1936) The Variation of Animals in Nature. London: Longman.
Rollo D (1994) Phenotypes: Their Epigenetics, Ecology, and Evolution. London: Chapman and
Hall.
Romanes GJ (189297) Darwin, and after Darwin: An Exposition of the Darwinian Theory and a
Discussion of Post-Darwinian Questions. Chicago: Open Court.
Ronshaugen M, McGinnis N, McGinnis W (2002) Hox protein mutation and macroevolution of

the insect body plan. Nature 416: 914917.
Roux W (1888) Beitr. Z. Entw. Mech. des Embryo. V. ber die knstliche Hervorbringung halber
Embryonen durch Zerstrung einer der beiden ersten Furchungszellen, soie uber die
Nachentwicklung der fehlenden Krperhalfte. Virchows Archiv 14: 419521.
Roux W (1905) Die Enwickelungsmechanik. Engelmann.
Rubinsztein DC, Amos W, Leggo J, Goodburn S, Ramesar RS, Old J, Bontrop R, McMahon R,
Barton DE, Ferguson-Smith MA (1994) Mutational bias provides a model for the evolution of
Huntington disease and predicts a general increase in disease prevalence. Nature Genetics 5:
524530.
Rudman WB (1981) The anatomy of alcyonarian feeding aeolid opisthobranch molluscs and
their development of symbiosis with zooxanthellae. Zool. J. Linn. Soc. 72: 219262.
Rumpho ME, Summer EJ, Meinhart JR (1999) Solar-powered sea-slugs: Mollusc-algal chloroplast
symbiosis. Plant Physiology 123: 2938.
Rupert JL, Hochachka P (2001) Genetic approaches to understanding human adaptation to

altitude in the Andes. J. Exptl. Biol. 204: 31513160.
Ruse M (1996) Monad to Man. The Concept of Progress in Evolutionary Biology. Cambridge:
Ruse M (1997) Huxley and evolution as science. In Thomas Henry Huxleys Place in Science and
Letters, ed. Barr A. Atlanta: University of Georgia Press.
Bibliography 495
Rutherford SL, Lindquist S (1998) Hsp90 as a capacitor for morphological evolution. Nature 396:
336342.
Saint-Andr A von, Blackwell NM, Hall LR, Hoerauf A, Brattig NW, Volkmann L, Taylor MJ, Ford
L, Hise AG, Lass JH, Diaconu E, Perlman E (2002) The role of endosymbiotic Wolbachia bacteria
in the pathogenesis of riverblindness. Science 295: 18921895.
Salthe S (1985) Evolving Hierarchical Systems. New York: Columbia University Press.
Sapp J (1994) Evolution by Association. Oxford: Oxford University Press.
Saunders PT (1984) Development and evolution. In Beyond Neo-Darwinism, ed. Ho M-W,

Saunders P. London: Academic Press.
Savageau MA (1989) Are there rules governing patterns of gene regulation? In Theoretical
Biology, ed. Goodwin B, Saunders P. Edinburgh: Edinburgh University Press.
Schalling M, Hudson TJ, Buetow KH, Housman DE (1993) Direct detection of novel expanded
trinucleotide repeats in the human genome. Nature Genetics 4: 135139.
Schimper AFW (1885) Untersuchungen ber die Chlorophyllkrner und Farbkrper. Jahrbcher
fr wissenschaftliche Botanik 1: 247302
Schindewolf OH (1937) Beobachtung und Gedanken zur Deszendenzliehre. Acta Biother. Leiden.
3: 195212.
Schindewolf OH (1962) Neokatastrophismus? Zeits. Deutsch. Geol. Res. 114: 430435.
Schleiden MJ (1838) Beitrge zur Phytogenesis. Mllers Archiv fr Anatomie, Physiologie und
wissenschaftliche Medecin. Berlin.
Schmalhausen II (1949) Factors of Evolution. The Theory of Stabilizing Selection. Philadelphia:

Blackiston.
Schrdinger I (1944) What Is Life? Cambridge: Cambridge University Press.
Schubert M, Holland LZ (2005) The Wnt Gene Family and the Evolutionary Conservation of Wnt
Expression. Georgetown TX: Landes/Eurekah Pubmed.
Schueller G (1998) Stuff of life. New Scientist 159, no. 2151: 3035.
Schwann T (1839) Mikroskopische Untersuchungen ber die bereinstimmung in der Struktur

und dem Wachstum der Thiere und Pflanzen. Berlin.
Schwartz JH (1999) Sudden Origins: Fossils, Genes, and the Emergence of Species. New York:
Wiley.
Schwartz M, Vissing J (2002) Paternal inheritance of mitochondrial DNA. N. Engl. J. Med. 347:
576580.
Schwartz RM, Dayhoff MO (1978) Origins of prokaryotes, eukaryotes, mitochondria and chloro-
plasts. Science 199: 395403.
Segre GV, Goldring SR (1993) Receptors for secretin, calcitonin, parathyroid hormone (PTH)/PTH-
related peptide, vasoactive intestinal peptide, glucagonlike peptide 1, growth hormone-releasing
hormone, and glucagon belong to a newly discovered G-protein-linked receptor family. TEM 4:
309314.
496 Bibliography
Seilacher A, Bose, PK, Pfluger F. 1998. Triploblastic animals more than 1 billion years old: Trace
fossil evidence from India. Science 282: 8083.
Severtsov AN (1927) ber die Beziehungen zwischen der Ortogenese und der Phylogenese der
Tiere. Jena Z. Naturw. 63: 51180.
Severtsov AN (1931) Morphologische Gesetzmssigkeiten der Evolution. Vienna: Fischer.
Severtsov AN (1934) Glavnye napravleniia evoliutsionnogo protsessa [Principal directions of the

evolutionary process], second edition. Leningrad: Biomedgiz.
Severtsov AN (1939) Morfologicheskie zakonomernosti evoliutsii [Morphological laws of

evolution], second edition. Moscow: Izdatelstvo Akademii nauk SSSR.
Shapere D (1980) The meaning of the evolutionary synthesis. In The Evolutionary Synthesis, ed.
Mayr E, Provine W. Cambridge: Harvard University Press.
Shapiro JA (1977) DNA insertion elements and the evolution of chromosome primary structure.
Trends in Biochem. Sci. 2: 622627.
Shapiro JA (1984) Observations on the formation of clones containing araB-lacZ cistron fusions.
Molecular and General Genetics 194: 7990.
Shapiro JA (1988) Bacteria as multicellular organisms. Sci. Am. 258, June: 8289.
Shapiro JA (1992) Natural genetic engineering in evolution. Genetica 86: 99111.
Shea BT (1988) Heterochrony in primates. In Heterochrony in Evolution, ed. McKinney M. New

York: Plenum.
Shelley M (1818) Frankenstein: or, the Modern Prometheus. Lackington, Hughes, Harding, Mavor
and Jones.
Sheppard PM (1958) Natural Selection and Heredity. Hutchinson.
Sherman PW, Jarvis JUM, Alexander RD, eds. (1992) The Biology of the Naked Mole-Rat.
Princeton: Princeton University Press.
Sherrington CS (1906) The Integrative Nature of the Nervous System. New Haven: Yale University
Press.
Shostak S, Kolluri V (1995) Symbiotic origins of cnidarian cnidocysts. Symbiosis 19: 119.
Simon JH (1962) The architecture of complexity. Proc. Am. Phil. Soc. 106: 462482.
Simpson GG (1944) Tempo and Mode in Evolution. New York: Columbia University Press.
Simpson GG (1953) The Major Features of Evolution. New York: Columbia University Press.
Sinha C (1987) Adaptation and representation: The role of ontogenesis in human evolution and
development. In Behaviour as One of the Main Factors of Evolution, ed. Leonovicov V, Novak
V. Prague: Czechoslovak Academy of Sciences.
Skolimowski H (1974) Problems of rationality in biology. In Studies in the Philosophy of Biology,

ed. Ayala F, Dobzhansky T. London: Macmillan.
Slijper EJ (1942) Biologic-anatomical investigations on the bipedal gait and upright posture in
mammals, with special reference to a little goat, born without forelegs. I, II. Proc. Koninkl. Ned.
Akad. Wetensch. 45: 407415.
Bibliography 497
Smith GT, Brenowitz EA, Wingfield JC (1997) Seasonal changes in the size of the song control
nucleus HVC revealed by multiple labels. J. Comp. Neurol. 38: 253261.
Smocovitis VB (1996) Unifying Biology: The Evolutionary Synthesis and Evolutionary Biology.
Princeton: Princeton University Press.
Smolin L (1995) The Life of the Cosmos. New York: Oxford University Press.
Smuts JC (1926) Holism and Evolution. London: Macmillan.
Snow CP (1959) The Two Cultures. Cambridge: Cambridge University Press.
Sol R, Goodwin BC (2000) Signs of Life: How Complexity Pervades Biology. New York: Basic
Books.
Spemann H (1914) ber verzogerte Kernversorgung von Keimteilen. Verh. d. D. Bool. Ges.
Freiburg 216221.
Spemann H (1938) Embryonic Development and Induction. New Haven: Yale University Press.
Hafner reprint (1962).
Spencer H (1852) The Development Hypothesis. The Leader.
Spencer H (18641866) Principles of Biology. London: Williams & Norgate.
Sperry RW (1979) Mental phenomena as causal determinants. In Consciousness and the Brain,
ed. Globus G, Maxwell G, Savodnik I. New York: Plenum.
Sperry RW (1983) Science and Moral Priority: Merging Mind, Brain, and Human Values. New
York: Columbia University Press.
Sperry RW (1991) In defence of mentalism and emergent interaction. J. Mind and Behavior 12:
221245.
Spiegelman S (1967) An in vitro analysis of a replicating molecule. American Scientist 55:

221264.
Srivastava RS (1968) Sri Aurobindo and the Theories of Evolution. Sanskrit Office, Chonkhamba.
Stanley SM (1979) Macroevolution: Pattern and Process. San Francisco: Freeman.
Starr DJ, Cline TW (2002) A host-parasite interaction rescues Drosophila oogenesis defects. Nature
418: 7679.
Stearns SC (1992) The Evolution of Life Histories. Oxford: Oxford University Press.
Stebbins GL (1974) Adaptive shifts and evolutionary novelty: A compositional approach. In

Studies in the Philosophy of Biology, ed. Ayala F, Dobzhansky T. London: Macmillan.
Stebbins GL (1982) Darwin to DNA, Molecules to Humanity. San Francisco: Freeman.
Steele EJ (1977) Somatic Selection and Adaptive Evolution. Toronto: Williams & Wallace.
Steinberg M (2003) Cell adhesive interactions and tissue self-organization. In Origination of

Organismal Form, ed. Mller G, Newman S. Cambridge: MIT Press.
Stent G (1969) The Coming of the Golden Age. Garden City NY: Natural History Press.
498 Bibliography
Stephens SG (1951) Possible significance of duplications in evolution. Advances in Genetics 4:

247265.
Stewart C-B, Wilson AC (1987) Sequence convergence and functional adaptation of stomach
lysozymes from foregut fermenters. Cold Spring Harbor Symp. Quant. Biol. 52: 891899.
Stewart I, Cohen J (1997) Figments of Reality. Cambridge: Cambridge University Press.
Stiassny MIJ (1991) Phylogenetic intrarelationships of the family Cichlidae: An overview. In

Cichlid Fishes, ed. Keenleyside M. London: Chapman and Hall.
Stiassny MIJ, Meyer A (1999) Cichlids of the rift lakes. Sci. Am. 280, February: 6469.
Suess E (1875) Eine Entstehung der Alpen. Braunmller.
Sulston JED, Schierenberg E, White JG, Thomson JN (1983) The embryonic cell lineage of the
nematode Caenorhabditis elegans. Dev. Biol. 100: 64119.
Sumnyj VK, Ruvinskij AO (1989) In memory of Dimitrij Constantinovic Beljaev. In Behaviour as

One of the Main Factors of Evolution, ed. Leonovicov V, Novk V. Prague: Czechoslavak
Academy of Sciences.
Sunquist F (1996) Two species, one design. International Wildlife Magazine. September-October:
1020.
Surani AM (2001) Reprogramming of genome function through epigenetic inheritance. Nature

414: 122128.
Sutherland GR, Haan EA, Kremer E, Lynch M, Pritchard M, Yu S, Richards RI (1991) Hereditary
unstable DNA: A new explanation for some old genetic questions? Lancet 338: 289291.
Sutovsky P, Moreno R, Ramalho-Santos J, Schatten G (1999) Ubiquitin tag for sperm

mitochondria. Nature 402: 371372.
Sykes B (1999) The molecular genetics of European ancestry. Phil. Trans. Roy. Soc. B 354:
131139.
Symonds N (1994) Directed mutation: A current perspective. J. Theor. Biol. 169: 317322.
Szalay FS (1998) Review of Widamaier EP (1998) Why Geese Dont Get Obese: How Evolutions
Strategies for Survival Affect Our Everyday Lives. San Francisco: Freeman.
Szathmry E, Maynard Smith J. 1995. The major evolutionary transitions. Nature 374: 227232.
Tartof KD (1974) Unequal mitotic sister chromatid exchange as the mechanism of ribosomal RNA
gene magnification. Proc. Natl. Acad. Sci. 71: 12721276.
Tatewaki M, Provasoli LX, Pintner IJ (1983) Morphogenesis of Monostroma oxypermum (kutz) Doty
(Chlorophyceae) in axenic culture, especially in bialgal culture. Phycology 19: 409416.
Taylor JS, Raes J (2005) Small-scale gene duplications. In The Evolution of the Genome, ed.
Gregory T. Amsterdam: Elsevier.
Teilhard de Chardin P (1955) Le Phnomne humain. Paris: Seuil.
Teilhard de Chardin P (1959) The Phenomenon of Man. London: Harper and Row. Harper
Torchbook edition, 1961.
Bibliography 499
Tepper S (1998) Six Moon Dance. New York: Avon.
Thaler DS (1994) The evolution of genetic intelligence. Science 264: 224225.
Thao ML, Gullan PJ, Baumann P (2002) Secondary (-Proteobacteria) endosymbionts infect the
primary (-Proteobacteria) endosymbionts of mealybugs multiple times and coevolve with their
hosts. Appl. Environ. Microbiol. 68: 190197.
Thom R (1972) Stabilit structurelle et morphogense: Essai dune thorie gnral des modles.
Reading: Benjamin.
Thompson DW (1917) On Growth and Form. Cambridge: Cambridge University Press. Second
edition: 1942.
Thompson JN (1989) Concepts of coevolution. Trends in Ecology and Evolution 4, June:

179183.
Thomson KS (1966) The evolution of the tetrapod middle ear in the rhipidistian-tetrapod
transition. Am. Zool. 6: 379397.
Thomson KS (1988) Morphogenesis and Evolution. Cambridge: Cambridge University Press.
Thomson KS (1992) Macroevolution: The morphological problem. Am. Zool. 32: 106112.
Tiffney BH (1981) Diversity and major events in the evolution of land plants. In Paleobotany,
Paleoecology and Evolution, volume 1, ed. Niklas K. Praeger.
Ting CN, Rosenberg MP, Snow CM, Samuelson LC, Meisler MH (1992) Endogenous retroviral
sequences are required for tissue-specific expression of a human salivary amylase gene. Genes
Dev. 6: 14571465.
Tittiger C, Whyard S, Walker VK (1993) A novel intron site in the triosephosphate isomerase gene
in the mosquito Culex tarsaslis. Nature 361: 470472.
Todd NB (1970) Karyotypic fissioning and canid phylogeny. J. Theor. Biol. 26: 445480.
Todd NB (1999) Mammalian evolution: Karyotypic fission theory. In Environmental Evolution,

second edition, ed. Margulis L, Matthews C, Haselton A. Cambridge: MIT Press.
Todd NB (2001) Kinetochore reproduction underlies karyotypic fission theory: Possible legacy of
symbiogenesis in mammalian chromosome evolution. Symbiosis 29: 319327.
Tomarev S I, Callaerts P, Kos L, Zinovieva R, Halder G, Gehring W, Piatigorsky J (1997) Squid Pax-
6 and eye development. Proc. Natl. Acad. Sci. 94: 24212426.
Tramontin AD, Smith GT, Breuner CW, Brenowitz EA (1998) Seasonal plasticity and sexual
dimorphism in the avian song control system: Stereological measurement of neuron density and
number. J. Comp. Neurol. 396: 186192.
Tsarfaty I, Resau JH, Tulong S, Keydar I, Faletto DL, Vandewoude GF (1992) The met roto-
oncogene receptor and lumen formation. Science 257: 12581261.
Turner J S (2000) The Extended Organism: The Physiology of Animal-Built Structures. Cambridge:
Uexkll JJ von (1913) Bausteiner zu einer biologischen Weltanschauung. Munich.

500 Bibliography
Uexkll JJ von (1926) Theoretical Biology. New York: Harcourt Brace.
Uvarov B (1966, 1977) Grasshoppers and Locusts. Centre for Overseas Pest Research, London.
Uzell T, Spolsky C (1974) Mitochondria and plastids as endosymbionts: A revival of special

creation? Am. Sci. 62: 334343.
Valentine JW (1986) Fossil record of the origin of bauplane and its implications. In Patterns and
Processes in the History of Life, ed. Raup D, Jablonski D. New York: Springer.
Valentine JW (1995) Late Precambrian bilaterians: Grades and clades. In Tempo and Mode in
Evolution, ed. Fitch W, Ayala F. Washington: National Academy Press.
Van Borm S, Billen J, Boomsma JJ (2002) The diversity of microorganisms associated with
Acromyrmex leafcutter ants. BioMed Central Evolutionary Biology 2: 926.
Van Valen L (1965) Morphological variation and width of the ecological niche. American
Naturalist 94: 377390.
Van Valen L (1973) A new evolutionary law. Evol. Theory 1: 130.
Vendruscolo M, Dobson CM (2005) A glimpse at the organization of the protein universe. Proc.
Natl. Acad. Sci. 102: 56415642.
Vernadsky VI (1926) Biosfera. Leningrad: Nauka.
Vernadsky VI (1998) The Biosphere. New York: Copernicus.
Verrengia J (1998) Associated Press report. Victoria Times-Colonist, November 26.
Virchow R (1858) Die Cellular-pathologie in ihrer Begrndung auf physiologische und patholo-
gische Gewebelehre. Berlin.
von Neumann J (1966) Theory of Self-Reproducing Automata. University of Illinois Press.
Vrba ES (1980) Evolution, species and fossils: How did life evolve? S. Afr. J. Sci. 76: 6184.
Vrba ES (1985a) Environment and evolution: Alternative causes of the temporal distribution of
evolutionary events. S. Afr. J. Sci. 81: 229236.
Vrba ES (1985b) The hierarchical expansion of sorting and selection: Sorting and selection cannot
be equated. Paleobiology 12: 217228.
Vrba ES (1989) What are the biotic hierarchies of integration and linkage? In Integration and
Evolution in Vertebrates, ed. Wake D, Roth G. New York: Wiley.
Vrba ES (1995) On the connections between paleoclimate and evolution. In Palaeoclimate and
Evolution, ed. Burckle L, Denton G, Partridge T. New Haven: Yale University Press.
Vrba ES (2004) Eco-evo-devo and the fossil record. In Environment, Development and Evolution,
ed. Hall B, Pearson R, Mller G. Cambridge: MIT Press.
Vrba ES, Burckle LH, Denton GH, Partridge TC, eds. (1995) Palaeoclimate and Evolution. New
Vrba ES, Eldredge N (1984) Individuals, hierarchies and processes: Towards a more complete evo-
lutionary theory. Paleobiology 10: 146171.
Bibliography 501
Vrba ES, Gould SJ (1986) The hierarchical expansion of sorting and selection: Sorting and
selection cannot be equated. Paleobiology 12: 227228.
Waagen W (1869) Die Formenreiche des Ammonites subradiatus. Geognostisch

Palaeontologischen Beitragen 2: 179256.
Waddington CH (1942) Canalisation of development and the inheritance of acquired character-

istics. Nature 150: 563565.
Waddington CH (1952) Genetic assimilation. Nature 169: 278.
Waddington CH (1953) The Baldwin effect, genetic assimilation and homeostasis.

Waddington CH (1956) The genetic basis of the assimilated Bithorax stock. J. Genetics 55:
240245.
Waddington CH (1957) The Strategy of the Genes. London: Allen & Unwin.
Waddington CH (1961) Genetic assimilation. Advances in Genetics 10: 257293.
Waddington CH (1966) The modular principle and biological form. In Module, Proportion,
Symmetry, Rhythm, ed. Kepes G. New York: Braziller.
Waddington CH (1968) Paradigm for an evolutionary procession. In Towards a Theoretical

Biology, volume 2, ed. Waddington C. Edinburgh: Edinburgh University Press.
Wagner GP (1989) The origin of morphological characters and the biological basis of homology.
Evolution 43: 11571171.
Wake D, Roth G (1989a) Complex Organismal Functions: Integration and Evolution in

Vertebrates. New York: Wiley.
Wake D, Roth G (1989b) The linkage between ontogeny and phylogeny in the evolution of
complex systems. In Complex Organismal Functions, ed. Wake and Roth. New York: Wiley.
Wake MH (1989) Phylogenesis of direct development and viviparity in vertebrates. In Wake D,

Roth G, Complex Organismal Functions. New York: Wiley.
Wake MH (2004) Environment, embryonization and viviparity. In Environment, Development

and Evolution, ed. Hall B, Pearson R, Mller G. Cambridge: MIT Press.
Waldrop MM (1992) Complexity: The Emerging Science at the Edge of Order and Chaos. New
York: Simon & Schuster.
Wallace AR (1858) On the tendency of varieties to depart indefinitly from the original type. J.
Proc. Linn. Soc (Zool.) 3: 5362.
Wallace AR (1870) Contributions to the Theory of Natural Selection. London: Macmillan.
Wallis M (1996) The molecular evolution of vertebrate growth hormones: A pattern of near-stasis
interrupted by sustained bursts of rapid change. J. Mol. Evol. 43: 93100.
Wallis M (2000) Episodic evolution of protein hormones: Molecular evolution of pituitary

prolactin. J. Mol. Evol. 50: 465473.
502 Bibliography
Watson DMS (1926) The evolution and origin of the Amphibia. Phil. Trans. Roy. Soc. B121:
4379.
Watson JD, Crick FHC (1953) Molecular structure of nucleic acids: A structure for deoxyribose
nucleic acid. Nature 171: 737738.
Webster G, Goodwin BC (1984) A structuralist approach to morphology. Rivista di Biologia 77:

503532.
Weele C van der (1999) Images of Development: Environmental Causes in Ontogeny. Albany NY:
State University of New York Press.
Weismann A (1885) Die Kontinuitt des Keimplasmas als Grundlge einer Theorie der Vererbung.
Jena: Fischer.
Weismann A (1893) The Theory of the Germ Plasm. London: Scott.
Weissbach A (1993) A chronicle of DNA methylation (19481975). In DNA Methylation, ed. Jost
J, Saluz H. Birkhauser.
Weitz CA, Garruto RM, Chin CT, Liu JC, He X (2000) Growth of Qinghai Tibetans living at three
different high altitudes. Am. J. Phys. Anthrop. 111: 6988.
Weldon WFR (1890) The variations occurring in certain decapod Crustacea. 1. Crangon vulgaris.
Proc. Roy. Soc. 47: 445453.
Wells WC (1819) An Account of a Female of the White Race of Mankind, Part of whose Skin
Resembles that of a Negro, with some Observations of the Cause of the Differences in Colour and
Form between the White and Negro Races of Man. London: Constable.
Weng G, Bhalla US, Lyenger R (1999) Complexity in biological signaling systems. Science 284:
9296.
Wesson R (1991) Beyond Natural Selection. Cambridge: MIT Press.
West-Eberhard MJ (1989) Phenotypic plasticity and the origins of diversity. Ann. Rev. Ecol. Syst.
20: 249278.
West-Eberhard MJ (2003a) Ryuichi Matsuda: A tribute and a perspective on pan-environmental-

ism. In Environment, Development and Evolution, ed. Hall B, Pearson R, Mller G. Cambridge:
MIT Press.
West-Eberhard MJ (2003b) Developmental Plasticity and Evolution. Oxford: Oxford University

Press.
Wheeler WM (1911) The ant colony as an organism. J. Morph. 22: 307325.
Wheeler WM (1929) Emergent evolution and the development of societies. Scientific Monthly,
February. Reprinted in Wheeler, Essays in Philosophical Biology (Russell & Russell, 1939).
Whewell W (1840) The Philosophy of the Inductive Sciences. London.
Whitehead AN (1925) Science and the Modern World. London: Macmillan.
Whyte (1965) Internal Factors in Evolution. New York: Braziller. Social Science Paperbacks
edition: Associated Book Publishers, 1968.
Bibliography 503
Willett-Brozeki JE, Savul SA, Richey LE, Baysal BE (2001) Germ line insertion of mtDNA at the
breakpoint junction of a reciprocal constitutional translocation. Human Genet. 109: 216223.
Williams GC (1966) Adaptation and Natural Selection: A Critique of Some Current Evolutionary
Thought. Princeton: Princeton University Press.
Willis JC (1922) Age and Area: A Study of Geographical Distribution and Origin of Species.
Cambridge: Cambridge University Press.
Willis JC (1940) The Course of Evolution. Cambridge: Cambridge University Press.
Willmer E N (1960) Cytology and Evolution. New York: Academic Press.
Wilson DS (1975) A general theory of group selection. Proc. Natl. Acad. Sci. 72: 143146.
Wilson EB (1928) The Cell in Development and Heredity, third edition with corrections. London:
Macmillan.
Wilson EO (1975) Sociobiology. Cambridge: Belknap.
Wilson EO (1985) The sociogenesis of insect colonies. Science 228: 14891495.
Wilson EO (1998a) The biological basis of morality. Atlantic Monthly, April: 5370.
Wilson EO (1998b) Consilience: The Unity of Knowledge. New York: Random House.
Wilson LG (1970) Sir Charles Lyells Scientific Journals on the Species Question. New Haven: Yale
University Press.
Wimsatt WC (1979) Reductionism, levels of organization, and the mind-body problem. In

Consciousness and the Brain, ed. Globus G, Maxwell G, Savodnik I. New York: Plenum.
Wimsatt WC (1980) Reductionistic research strategies and their biases in the units of selection
controversy. In Scientific Discovery: Case Studies, ed. Nickles T. Dordrecht: Reidel.
Wimsatt WC (1986) Developmental constraints, generative entrenchment, the innate-acquired

distinction. In Integrating Scientific Disciplines, ed. Bechtel W. Martinus. The Hague: Nijhoff.
Wimsatt WC (1997) Aggregativity: Reductive heuristics for finding emergence. Phil. Sci. 64:
S372S384.
Wimsatt WC (1998) Simple systems and phylogenetic diversity. Phil. Sci. 65: 267275.
Wistow G (1993) Identification of lens crystallin: A model system for gene recruitment. Methods
in Enzymology 224: 563575.
Woese CR, Fox GE (1977) Phylogenetic structure of the prokaryotic domain: The primary
kingdoms. Proc Natl. Acad. Sci. 74: 50885090.
Wolff CF (1759) Theoria generationis. Berlin.
Wolff CF (1764) Theorie von der Generation, in zwo Abhandlungen erklrt und bewiesen. Berlin.
Wolffe AP, Matzke MA (1999) Epigenetics: Regulation through repression. Science 286: 481486.
Wood WB (1988) The Nematode Caenorhabditis elegans. Cold Spring Harbor Laboratory Press.
Woodger JH (1929) Biological Principles. London: Routledge and Kegan Paul.

504 Bibliography
Wray GA (1998) Promoter logic. Science 279: 18711872.
Wray GA, Levinton JS, Shapiro LH (1996) Molecular evidence for deep Precambrian divergences
among metazoan phyla. Science 247: 568573.
Wray GA, Raff RA (1989) Evolutionary development of cell lineage in the direct-developing sea
urchin Heliocidaris erythrogramma. Dev. Biol. 132: 458470.
Wray GA, Raff RA (1990) Novel origins of lineage founder cells in the direct developing sea urchin
Heliocidaris erythrogramma. Dev. Biol. 141: 4154.
Wright BE (2000) A biochemical mechanism for non-random mutations and evolution.

J. Bacteriol. 182: 29933001.
Wright S (1931) Evolution in Mendelian populations. Genetics 16: 97159.
Wright S (1932) The roles of mutation, inbreeding and crossbreeding, and selection in evolution.
In Proceedings of Sixth International Congress on Genetics, Ithaca.
Wurtele H, Little KC, Chartrand P (2003) Illegitimate DNA integration in mammalian cells. Gene
Ther. 21: 17911799.
Wynne-Edwards KE (1998) Evolution of parental care in Phodopus: Conflict between adaptations

for survival and adaptations for rapid reproduction. Amer. Zool. 38: 238250.
Wynne-Edwards KE, Surov AV, Telitina AY (1999) Differences in endogenous activity within the
genus Phodopus. J. Mammalogy 80: 855865.
Wynne-Edwards VC (1962) Animal Dispersal in Relation to Social Behaviour. Edinburgh: Oliver

& Boyd.
Yeats WB (1920) The Second Coming. In W. B. Yeats, Selected Poetry, ed. Jeffans A. London:
Macmillan.
Yoshida N, Oeda K, Watanabe E, Mikami T, Fukita Y, Nishimura K, Komai K, Matsuda K (2001)

Chaperonin turned insect toxin. Nature 411: 44.
Yuh C-H, Bolouri H, Davidson EH (1998) Genomic cis-regulatory logic: Experimental and com-
putational analysis of a sea urchin gene. Science 279: 18961902.
Yuh C-H, Bolouri H, Davidson EH (2001) Cis-regulatory logic in the endo16 gene. Development
128: 517629.
Zambryski P (1988) Basic processes underlying Agrobacterium-mediated DNA transfer to plant

cells. Ann. Rev. Genet. 22: 130.
Zambryski P (1989) Agrobacterium-plant cell DNA transfer. In Mobile DNA, ed. Berg D, Howe M.
American Society for Microbiology.
Zimmer C (1998) At the Waters Edge: Fish with Fingers. Whales with Legs. New York: Simon and
Schuster.
Zuckerkandl E (1975) The appearance of new structures and functions in proteins during
evolution. J. Mol. Evol. 7: 157.
Index
Accommodation Arber, A., 407

epigenetic, 194196 Archaeopteryx, 187
physiological, 144 Archetype, 294, 412, 418
Acquisition of heritable characteristics, 355 Arctic char, 343
Adaptability, 13, 68, 82, 294, 315, 403 Arctic fox, 55, 56, 151, 152
and adaptation, 140, 141 Ardisia, 122
human, 100, 331 Aristotelian holism, 82
Adaptationism, 37, 39 Aristotle, 72, 126, 128, 181, 317, 322
Adaptiveness, 7, 397 Aromorphosis, 155
Adaptive radiation, 30, 287, 411 Artemia, 245
Adaptive suites, 139 Arthropod appendage evolution, 412
Aggregation, 125 Arthur, W., 48, 216, 225, 273
Aggregativity, 316, 419 Artificial selection, 53, 56, 371
Agrobacterium tumefasciens, 20, 265 Ashby, W. R., 301
Albedo, 367 Associations, terminology of, 97
Alexander, S., 73, 318 Autocatalytic molecular systems, 160
Alexandrian schools, 133 Autoevolution, 307
Allometry, 47, 219, 267, 274, 275, 278, 279, Autonomization, 55, 176
356, 357, 365, 367, 374 Axolotl, 192
Allopolyploidy, 98 Aymara tribe, 203
Ammonite lobate lines, 269
Ammonium ions, 171 Babbage, C., 263
Anabaena, 127 Bacon, F., 62, 322, 329
Ancon ram, 183 Baconian and Darwinian epistemology, 361
Animated water, 351 Baconian induction, 361
Antennapedia, 245 Bacteriophages, 127
Anticipation diseases, 238, 272, 280 Bacteroides thetaiotamicron, 123
Ant lions, 101 Baer, K. E. von, 183
Ants, 101, 102, 129, 359 Bak, P., 74, 321
Aphids, 101 Baker, M. W., 239
Apoptosis, 235 Balfour, F. M., 185
506 Index
Balon, E. K., 196, 207, 208, 338, 343 Burrowing benthic animals, 349
Bardou, F., and Jaeger, L., 228 Buss, L., 215
Bateson, W., 4, 54, 64, 185, 341 Butler, S., 52
Beament, J. W., 149, 150
Behavior, 337339 C3 plants, 172
choices, 360 C4 plants, 172
genes for, 337 Cactus, 196
hereditary, 367 Caenorhabditis elegans, 211, 212, 371
Behe, M., 12, 249 Cairns-Smith, G., 161
Belyaev, D., 55, 56, 151 Callebaut, W., and Raskin-Gutman, D., 301
Bemisia tabaci, 102 Callinectes sapidus, 171, 295
Bnard cells, 321, 374 Camel, 145
Bergson, H., 318 Campbell, J. H., 223, 262
Bernard, C., 138, 145 Campbell, N., 307
Berry, C. V., 27 Canalization, 190
Bertalanffy, L. von, 6, 8 Candida albicans, 207
Beurlen, K., 155 Cannon, W., 138, 145
Bifurcation, 290 Caporale, L., 164, 225, 228
Big Bang, 16, 21, 85, 384, 426, 428 Cartilage formation, in limb buds, 197
Big Bang of Biology, 3, 25, 85 Catastrophe, 53, 81,175, 220, 326, 351, 359,
Biochemical evolution, 156158 366, 370, 405
Biochemical pathway switches, 172 Catastrophe insurance, 254
Biofilms, 127 Catastrophic stress, 255
Biological structuralism, 307 Cathepsins, 169, 170
Biological synthesis, 401 Caudwell, C., 74, 75
Biosphere, 350 Causal theory of evolution, 23
Birdness, 415 Causation
Bithorax, 185, 245 D. Hume and E. Darwin on, 57
Body plans proximate cause of evolution, 58, 406
bilaterally symmetrical, 8 proximate causes and ultimate effects, 317
radially symmetrical, 8 ultimate cause of evolution, 58, 294, 295, 406
universal, 344 Cell adhesion molecules, 108
Bolk, L., 268 Cell theory, 28
Bone morphological protein 2, 279 Cellulolytic symbiosis, 113,122, 336
Bonner, J., 256 Cellulose, 336, 367
Branchiostoma lanceolatum, 246 Cenancestor, 162
Brenner, S., 211, 372 Cenogenesis, 192, 246
Britten, R. J., and Davidson, E. H., 165, 278 Centriole, 105
Brooks, W. K., 185 Centromere, 107
Buchnera, 101 Cepaea nemoralis, 206
Burgess Shale, 6 Chaisson, E., 428
Burke, A. C., 197 Chambers, R., 263, 318
Burkhardt, R., Jr., 265 Change of function, 293
Index 507
Chaperonins, 101 Creodes (cell lineages), 195

Cheddar man, 12 Crespi, B., 127
Cheek pouches, in rodents, 197 Critical-point emergence, 74, 320, 367
Chemoton stage, 162 Crocodiles, 173
Child, C. M., 137 Croizat, L., 402
Chloroplast, 118, 175, 335, 341 Crossroads of evolutionary theory, 421
Chromatid break repair, 342 Crystallins, 170, 248
Chromatin marks, 251, 253 Cubomedusan, 248
Chromosome Curates egg, 427
amplification, 164 Cuvier, G., 2, 370
and sex, 104 Cyclic AMP, 168, 229
diminution and deletion, 237 Cytotaxis, 250
mutation, 107
puffs (Balbiani rings), 231 Dachshund, 183
Churchill, F., 38 Darwin, C. R., 203, 267, 345, 352, 366, 435
Chymotrypsin, 233 absence of natural selection, 53
Cichlid evolution, 416 artificial selection, 425
Circulatory system, 351 laws of growth, 272
Circus clowns, 345 monstrosities, 32, 54, 119
Coacervates, 160 natural selection as metaphor, 6
Co-adaptation, 342 natural selection as consequence of
Coelurosauravus jaekeli, 217, 320 Struggle for Life, 9
Co-evolution, 102 physiological adaptability, 46
Cohen, J., and Stewart I., 67, 71, 311, 360, 387 physiology, 138
Commensalism, 99 plasticity of organization, 54, 55
Competition, 34, 72, 134, 394, 426 retrogression, 5
Complexification, 115, 389, 402 species, 417
Complexity, 6870 Darwin, E., 16, 18, 212, 350
Conatus, 46 Davies, P., 281, 428
Concerted evolution, 240, 274 Dawkins, R., 22, 60, 61, 130, 249, 430
Condition of mutability, 243 De Beer, G., 192, 193, 246, 268
Conrad, M., 68, 140, 142, 143, 162 Deep homology, 246
Consilience, 129 De Vries, H., 54, 185
Constrained generating procedure, 313 Detoxifying gene duplication, 236
Contingencies, 286, 366 Developmental genetics, 38
Contingency-dependent emergences, 359 Developmental thresholds, 338
Cope, E. D., 4, 138, 146 Devolution, 395
Coral reefs, 112 Dialectical materialism, 361
Cormorant, 153 Dialectical synthesis, 364
Corning, P., 37, 77 Dictyostelium, 358
Corpus callosum, 309, 367 Differential persistence, 314
Cosmological evolution, 369, 426 Direct filiation theory, 119
Creationism, 2, 9, 31, 375 Directional exaggerations, 270
508 Index
Disequilibration, 360, 366 extrinsic (environmental), 74, 322, 324

Dissostichus mawsoni, 233 formulas, 92
Divergent saltations, 365 at interfaces, 381
Diversifying evolution, 15 intrinsic (autonomous), 74, 209, 322324
Djungarian hamster, 131, 151 by natural selection, 90
Dobzhansky, T., 38, 90 overview, 319
Dobzhansky, T., Ayala, F. J., Stebbins, G. L, pressure, 311
and Valentine, J. W., 8 and reductionism, 77
Dodo, 346 saltatory, 79, 80, 319, 359, 366, 367, 380
Dog evolution, 283 theses, and selectionist antitheses, 390398
Dog whelk morphs, 207 at thresholds, 196, 359
Dohrn, A., 354 Through the Looking Glass, 292
Dolly (sheep), 253 Emergence theory
DOrbigny, A., 203 empirical tests, 379
Dosage imbalance, 240 preliminary outline, 78
Dose amplification, 165 Emergent evolution
Dose repetition, 236 modes, 80
Douglas, A., 113, 116 rate, 410
Dover, G., 240, 260, 272, 281 Emergent properties, 13
Drummond, H., 73 constellation of, 145, 286
Dwarf animals, 282 and resultant properties, 71
Dwarfism, 187 Emergentism
Dynamic structure, 304 and causal theory of evolution, 86
definitions of terms, 398, 399
Ecdysone, 231 as evolutionary theory, 368
Ecological release, 52 and interactionism, 387
Ecostasis, 328, 366, 404 and neo-Darwinism, 93
Ecosystems and symbiogenesis, 111115 origins, 7275
Edge effect, 149 Emperor penguin, 152
Ediacarans, 213 Endler, J., 1, 43, 44
Eimer, T., 267, 268 Endo16, 263
Eldredge, N, 27, 39, 59 End of science, 435
Eldredge, N., and Gould, S. J., 50, 357 Endogenous retroviruses, 103
Eldredge, N., and Vrba, E., 402 Endosymbiosis, 98
Electronic evolution, 372 Entelechy, 189
El-Hani, C., and Pihlstrm, S., 81 Enterobacter aerogenes, 101
Eliot, T. S., 401, 406 Epigenesis, 181
Embryonization, 205 Epigenetics
Emergence accommodatory mechanism, 262, 341
contingency-dependent, 359 algorithms, 218, 219, 263, 264, 358, 371,
critical-point, 79, 80, 320 372
and dialectical synthesis, 390 burden, 303
and environmental contingencies, 88 deviation, 193
episodic, 366 effects of stress, 254
Index 509
effects of symbioses, 122 Fenchel, T., 411

effects of transposable elements, 242 Fenchel, T., and Riedl, R., 111
exploratory behavior, 200 Fetalization, 268
inheritance systems, 250257 Fiber theory, 28, 29, 40
mechanical stimuli, 217 Finches, Darwins, 414, 415
mechanisms, 258260 Fisher, R. A., 50, 185
plasticity, 188 Fitness, 33, 395, 423
thresholds, 320, 343 Fleming, A., and Allison, V. C.,170
Epiphenomena, 418 Flight, as critical-point emergence, 375
Epistemological monsters, 436 Fondon, J., and Garner, H., 197, 283
Epitrichal glands, 298 Forbes, E., 203
Escherichia coli, 228 Founder effect, 51
Essentialists, 388 Fragile-X, 280
Euglena, 103 Frankenstein, 29
Eukaryote emergence, 116 Frankov, A., 338
Eusociality, 110, 125 Fugu rubripes, 236
Evo-devos, 47 Functionswechsel, 354
Evolution
accelerated in hominins, 10 Gaia, 89, 350
behavioral, 337339 Gaian evolution, 430
by association, 330, 331 Galactosidase, 229
developmental, 339344 Galen, 72, 133
in spite of natural selection, 24 Galton, F., 49
neo-Darwinist definition, 36 Gannet, 141
physiological, 334337 Garstang, W., 192, 209
Evolutionary avalanche, 293 Gehring, W., 92, 211, 247
Evolutionary effects of external environment, Gene amplification, 164
348 Gene conversion, 240
Evolutionary experiments, 8 Gene pool, 11, 45
Evolutionary isms, 3 General theory of biology, 303
Evolutionary psychology, 110, 127, 129, 337, Generative conditions, 285, 366, 333, 334
339 Generative entrenchment, 303, 341
Evolutionary stable strategy, 34 Generative procedures, 385
Evolvability, 84, 219 Generative hypotheses of evolution, 14
Exaptation, 148, 354 Genetic accommodation, 204
Exons, 228, 232 Genetic assimilation, 155, 201, 357
Exon shuffling, 233 Genetic drift, 51
Extinctions, 239 Genetic drive, 278
Extrinsic emergence, 324 Genocopying, 208
Eyeless, 212 Genophore, 104
Geophysiology, 350
Farmer, D., 382 Gerhart, J., and Kirschner, M., 243, 248, 414
Fat body, 171 Ghiselin, M., 277, 420
510 Index
Giant animals, 282 Hall, B. K., 197, 202, 216, 225, 344
Giantism, 187 Hall, T. S., 263
Gifford lectures, 73 Halteres, 245
Gilbert, S., 301 Hamburger, V., 48
Gill arches, 314, 416 Hardy, A., 193
Giraffes neck, 279 Hawkes, N., 1
Global warming, 121 Heat-shock proteins, 235
Glossinia, 100 Hegel, G. W. F., 72
Glycolysis, 172 Hegelian doctrine, 361
Glycoprotein antifreeze, 234 Helix aspersa, 206
Goethe, J. W. von, 181 Hemocyanin, 171
Goldschmidt, R., 43, 51, 186, 208, 224, 268 Hemoglobin, 169, 174
Goldschmidt toad, 187 Hens teeth, 250
Goodrich, E. S., 193 Heslop-Harrison, J., 272
Goodwin, B. C., 1, 23, 71, 91, 214, 215, 248, Heterochrony, 184, 355
249, 432, 433 Heterorhesis, 190
Gottlieb, G., 146, 147, 338 Hierarchies
Gould, S. J., 14, 192, 198, 250, 289, 382, 428 compositional, 300, 386
Gould, S. J., and Lewontin, R., 37 control, 386
Gout, 173, 424 and emergent levels, 299303
Gradualism, 3, 48 focal level, 300
Grant, P., and Grant, R., 414 generative level, 300
Grass, P. -P., 4, 276 and levels of selection, 299
Grehan, J., 272 High table of selectionism, 10
Grehan, J., and Ainsworth, R., 271, 284 Himmelfarb, G., 42
Greksa, L. P., 203 Hippocratic medicine, 133
Grene, M., 421 His, W., 198
Grizzly bears, 387 Historical layering, 386
GroEL, 101 Historical theory of evolution, 23
Group, 125 History of ideas, 291
Groups, as wholes, 419 Ho, M. -W., 179, 180, 208
Group selection hypothesis, 318 Ho, M. -W., and Saunders, P., 179, 180
Growth hormone, 167, 239 Hoatzin, 346
Gut functions, 148 Holland, J., 22, 67, 73, 76, 312314, 335, 344,
363, 371, 375, 385, 434
Haake, W., 268 Holobiosis, 98
Haeckel, E., 198 Holon, 301
Haemophilus influenzae, 237 Homeoboxes, 244
Haines, L. R., 100 Homeodynamics, 147
Hair, 298 Homeorhesis, 189, 220, 327, 340
Hair glands, 148 Homeostasis, 145, 146, 327, 328, 340, 353,
Haldane, J. B. S., 38 413
Haldanes aphorism, 431 Homeothermy, dinosaur and avian, 298
Index 511
Homeotic genes, 244 Jegalian, K., and Lahn, B., 257

Homo floresiensis, 282 Jennings, H. S., 95, 109, 405, 432
Homologous recombination repair, 235 Jokes, 434
Homology, 30, 218 Junk DNA, 223, 236
Hopeful monster, 186, 283, 422
Horgan, J., 385 Kangaroo, 194
Horse, 270, 276 Kant, I., 72
Hox, 164, 244, 320, 344 Karyomastigont, 117
Hughes, Q. J., and Lambert, D., 407 Karyotype fission theory, 108
Human genome project, 11 Kauffman, S., 59, 76, 159, 249, 271, 289, 323,
Huntingtons disease, 238 324, 384, 438
Hutton, J., 350 Keller, E. F., 199, 271, 410
Huxley, J., 21, 38, 47, 137, 268, 275, 296, 363, Key innovations, 83, 285, 298, 373
378, 402 Kim, J., 77
Huxley, T. H., 73, 182, 184 Kimura, M., 51, 52
Hydraulic mechanisms, 351 Kinetosome, 106
Hydrostatic pressure, 198 King, D., 238
Hydrothermal vents, 158 King, R. C., and Stansfield, W. D., 202
Hylozoism (panpsychism), 48, 319, 384, 424, Kingsolver, J. G., 409
427, 428, 429 Kirschner M., and Gerhart J., 143, 200, 225,
Hypermorphosis, 367 344
Kludges, 5
Imaginal discs, 246 Koch, A. L., 254
Imprinting, 252 Koch, C., and Laurent, G., 348
Insects Koestler, A., 191, 301, 432, 434
evolution, 412, 413 Kollar, E. J., and Fisher, C., 250
wings, 245 Klliker, R. A. von, 183
Insertion sequences, 241 Kolnicki, R., 108
Integrins, 109 K-T (Cretaceous-Tertiary boundary), 3, 276,
Intelligence, 367 412
Intelligent design, 9, 249, 381 Kuhn, T. S., 28
Interactionism, 12, 75, 264
Interference RNA, 230 Labyrinthodont amphibia, 275
Internal milieu, 347 Lac operon, 228
Interphene, 198 Lactose, 229
Interspecific epigenetics, 344 Lactose synthetase, 170
Intolerant abstraction, 70, 157 Lamarck, J. -B., 3, 17, 29, 46, 130, 151, 177,
Intragenic recombination, 232 220, 266, 347, 363, 402
Introns, 232 Lamarckism, 3, 265, 347
Isoenzymes, 165 Lamprey, 246
Language, 131
Jablonka, E., and Lamb, M., 166, 202, 225, 250, Laysan duck, 254
251, 253, 256, 262 Levit, G., and Hossfeld, U., 269
512 Index
Lewes, G. H., 71 McGinnis, W., 245

Lewontin, R., 345, 346 McMenamin, M., 213
Li, W. -H., and Graur, D., 225, 240 Mealybug, 102
Lichens, 99 Medawar, P., 208
Light stimulation of development, 348 Megaceros, 275
Lima-de-Faria, A., 94, 307, 383 Membrane receptor molecules, 109
Limblessness, 187 Meme concept, 120
Linde, A., 429 Metamorphosis, 183, 246, 412
Livant, W., 11 Metaphors
Lobe fins, 247 biological, 19
Locusts, 176, 177, 188, 349 emergentistic, 87
Logic, 132 religious, 61
Logsdon, J. F., and Doolittle, R. F., 234 Methylation, 251
Looking Glass logic, 63, 72, 78 Methyl transferase, 252
Lotka, A., 428 Metz, C. W., 296
Lovejoy, A., 291, 309 Mill, J. S., 72, 374
Lovelock, J., 89, 350 Milne Edwards, H., 295
Lvtrup, S., 47, 63, 181, 199, 224, 225, 275 Mind, 390, 433
Lucinoid bivalves, 411 Mitochondria, 117, 124, 174
Luck, 51 Mitosis, 106
Lung capacity, 203 Mitotic spindle, 105
Luther, M., 61 Mivart, St. G. J., 4, 50, 138, 267, 282, 357,
Lwoff, A., 173 402
Lyell, C., 4 Mix-match principle, 95, 284, 354
Lymantria, 186 Modern synthesis, 2,19, 23, 38, 40, 67, 364,
Lysosomes, 169 423
Lysozyme, 170 Modularity, 81, 301
Molecular adaptability, 205
Mackie, G., 248 Molecular clock, 410
Manx cat, 187 Molecular drive, 240, 274
MAP-kinase, 163 Monk, M., 250, 252
Margulis, L., 95, 105, 111, 116, 118 Monkey parable, 17, 430
Margulis, L., and Sagan, D., 108, 117 Monod, J., 36
Marxist doctrine, 361 Monstroma, 122
Matsuda, R., 192, 196, 201, 205, 207, 223, Morgan, C. L., 21, 73, 132, 184, 321, 322, 374
264, 343 Morowitz, H., 318
Maynard Smith, J., 296 Morphogenetic fields, 424
Maynard Smith, J., and Szathmry, E., 22, 60, Mouse gut epigenesis, 123
133, 297 Muller, H. J., 19, 158
Mayr, E., 38, 39, 40, 58, 292295 Mller, G. B., 196, 198, 199, 200, 340
Mayr, E., and Provine, W., 47 Mller, G. B., and Wagner, G., 179, 180, 309,
McClintock, B., 51, 108, 224, 254, 296 310, 340
McDougall, W., 427 Multicellularity, 212219
Index 513
Multifunctionality of emergents, 147, 286, Neural crest cells, 168, 197, 216, 247, 373
314 New biology, 422
Murphy, J. J., 137 New genes, 169
Mutation theory, 32, 48 Newman, S. A., and Mller, G. B., 207, 209,
Mycorrhizae, 113 215, 217, 218, 223, 249, 257, 338, 388
Myoglobin, 169 Nicolis, G., and Prigogine, I., 321
Myotonic dystrophy, 238, 280 Niklas, K., 118
Myrmeliontidae, 101 Nitrogen cycles, cellular, 173
Mystacina tuberculata, 321 Nitrogen fixation, 99,127
Nod factors, 122
Naked gene hypothesis, 158 Non-homologous recombination, 235
Naked mole rat, 153 Non-random hypermutability, 164
Natural experiment, 19, 80, 87, 297, 322, 351, Norton, H. T. J., 32
421 Null-hypothesis experiments, 56, 380
Natural selection. See also Darwin, C. R. Numbers of differentiated cell types, 389
absence of, 371 Nsslein-Volhard, C., 214, 215
as barrier to evolution, 407 Nuttallia obscurata, 144
as book-keeping, 67
destabilizing, 55, 379 Octopus, 335
as differential survival and reproduction, 9, Odell, G., 199, 200, 410
33 Ohno, S., 165, 301
directional, 269 Ontogenic buffering, 195
disruptive, 409 Ontogenic plasticity of plants, 335
as filter, 27 Oparin, A. I., 160
of groups, 420 Operator, 228
as hypostasis, 5, 423 Organophosphorus hydrolase, 170
internal, 55 Orgel, L., 159
in the wild, 43 Origin of life, 157164, 351
normalizing, 55 Orthogenesis, 247, 413
pre-Darwinian, 2 and anticipation diseases, 280
as secular creator, 38 and exaggeration of hereditary traits,
of species, 420 273275
as syndrome of causes and effects, 80 and genetic drive, 278, 279
stabilizing, 10, 34 and laws of growth, 267, 268
units of, 418 Orthoselection, 269
Nature philosophy, 181 Osborn, H. F., 202, 203
Navier-Stokes equations, 374 Oscines brains, 294
Nelson, G., 402 Osmoregulation, 171, 148
Nematocyst, 112 Ostrich calluses, 358
Neo-Lamarckism, 3, 31, 177, 220, 266, 347 Otter, 187
Neo-Lamarckist process, 253 Overprinting, 233
Neophobism, 415 Owen, R., 181, 295
Neumann, J. von, 158 Oyama S., 12, 75, 208, 263, 290, 308
514 Index
Paedomorphosis, 191, 192, 243, 343 Popper, K., 56, 380

Pan, 226 Population thinking, 44, 266
Pandas thumb, 198, 309 Position effects, 107, 224, 243
Panpsychism. See Hylozoism Post-Lamarckists, 368
Paradigms, 28 Postmodernism, 16, 6264, 422
Paraheredity, 98 Post-prediction, 375
Parasitism, 103 Post-transcriptional gene silencing by RNA,
Parrots 230
African grey, 415 Poulton, E. B., 32
kakapo, 346 Pray, L., 254
kea, 415 Predictability of emergence, 373375
Pax, 247 Predictable emergences, 376378
Pearson, R. D., 147, 176 Predictiveness of emergence theory, 373375
P-element, 281 Proctotrupid wasps, 150
Peramorphosis, 192 Progenesis, 192
Permease, 229, 250 Progenote stage, 162
Persistent patterns, 314, 387 Progress, 17, 60, 403
Personal knowledge, 434 Progressionism, 17, 406
Pfeisteria, 127 Progressive evolution, 17, 406
Phase transitions, 358 Prolactin, 167, 192, 239
Phenocopying, 208 Promoter sequence, 228
Pheromones, 176 Prosser, C. L., 432, 433
Phocomelic condition, 187 Protein
Phodopus campbelli, 151 domains, 233
Phodopus sungorus, 151 storage, 170, 171
Phosphoenolpyruvate, 172 tertiary structure, 228
Photosynthetic ecosystems, 112 Protobionts, 161
Physical gill, 150 Provine W., 38, 425, 426
Physiogenesis, 146, 154, 155, 334 Pseudogene, 238
Physiological evolution, 137, 138, 333337 Pteranodon, 218
Phytoplankton, 166 Pteroid bone, 218
Piaget, J., 338 Pug dogs, 273
Pigeon sports, 182 Punctuated equilibrium, 21, 48, 375, 402
Plant-fungus ecosystems, 112 Punnett, R. C., 32
Plant physiology, 178 Pytho deplanatus, 351
Plate, L., 269
Platonic essentialism, 45 Qualities, science of, 91
Pleiotropic by-product, 293 Questiones disputatae, 63
Point mutation, non-synonymous, 227 Quetzalocatlus, 218
Polanyi, M., 308 Quorum sensing, 127
Pollinators, 103, 336
Polytene chromosomes, 231, 273 Raff, R., 197, 216, 278, 301
Popov, I., 269 Raff, R., and Kaufman, T. C., 196
Index 515
Rate of evolution, 20 Rupert, J. L., and Hochachka, P., 203

Reaction channeling, 163 Ruse, M., 39
Rebeck, J., 160
Recombinators, 230 Salivary amylase, 243
Redox interface, 121 Saltations, 50, 184, 245, 271, 276, 330
Red Queen, 327 Saltatory evolution, 48
Reduction, 11, 69 Salthe, S., 300, 306
Reductionism, 11, 70, 77, 423 Sapp, J., 97
Redundancy, 8, 376 Saunders, P., 190
Regression, physiological, 173 Schaffner, W., 238
Regulator gene, 229 Schmalhausen I., 10, 13, 35, 139, 146, 149,
Reid, C. E., 346, 415 150, 176, 190, 193, 296
Reid, R. G. B., 75, 271, 308, 341 Schubert, M., and Holland, L. C., 247
Reimchen, T., 206 Schwartz, D., 160, 161, 281
Rensch, B., 38, 47, 269, 276 Schwartz, J., 39, 316
Repair of double strand breaks in DNA, 238 Scottish covenanters, 61
Repair mechanisms, 234, 235 Second messengers, 168
Repatterning, epigenetic, 199 Segment polarity genes, 244
Repetitive differentiation, 164, 353 Segregators, 230
Repetitive DNA, 236 Seilacher, A., Bose, P. K., and Pfluger, F., 215
Replication slippage, 237 Selection pressure, 6, 35, 49, 52, 170, 171,
Repressor, 229 234, 241, 248, 294, 349, 396, 405, 423
Reproduction, 352 Selector genes, 230, 244
Respiration, 174 Selfish gene, 45
Retroposition, 241 Self-organization, 355
Retroposon, 242 Self-organized criticality, 74, 321
Retroviral gene acquisition, 355 Serial homology, 295
Retroviruses, 243 Sesamoid bones, 198
Reverse transcriptase, 159, 242 Severtsov, A., 146, 155
Rhinoceros, 276 Sex, 104
Rhizobium, 114, 127 Sex-determining region Y (SRY) gene, 257,
Ribozyme, 159 258
Riedl, R., 186, 196, 302, 303 Sexual reproduction, 257
Riftia, 111 Sexual selection, 419
Ring, R. A., 351 Shapere, D., 47
RNA polymerase, 228 Shapiro, J., 234, 261, 262
RNA world, 159 Sherrington, C. S., 138
Robson, G. C., and Richards, O. W., 7 Simon, J. H., 301
Robustness, Simpson, G. G., 38, 44, 270
epigenetic, 199, 200 Slijpers goat, 189
physiological, 141 Smocovitis, V. B., 39, 40
Rollo, D., 139, 302, 324, 376 Smolin, L., 429, 430
Romanes, G., 58 Social cohesiveness, 125
516 Index
Social compartmentalization, 126 Symbiodinium, 98, 99

Social connectedness, 125 Symbiogenesis, 97, 120
Social differentiation, 126 Symbiont, 97
Social integration, 126 Symbioplex, 97
Social permeability, 125 Symbiostasis, 121, 123, 327
Societies, 109111, 125 Symbiote, 97
Sodalis glossinidius, 100 Syndactyly, 186
Sol, R., and Goodwin, B. C., 128, 311, 369, Synergism hypothesis, 77, 317
371, 374 Synthesis, 40
Somatic mutation, 196 Systems reduction, 71, 124, 388
Sonic hedgehog, 279
Soredia, 99 Talitrid amphipods, 205
SOS repair system, 235 Telemorphosis, 153
Specialization bind, 191 Telomerase, 236
Speciation, 85, 243, 417, 418 Teratology, 183
Species selection, 420 Terminus genes, 244
Spemann, H., 185 Termites, 102
Spencer, H., 50, 184, 212 Theory of correlated variation, 185
Sperry, R., 75, 308 Theory of organic mechanism, 299
Spiegelmans monster, 281 Theory of serial endosymbiosis, 118
Spinoza, B., 46 Thermal vent, 111
Spliceosomes, 232 Thermodynamics, second law of, 382
Sponge cell reorganization, 358 Thermogenesis, 332
Sports, 54, 56, 182 Thermoplasma, 116, 117
Stable evolutionary strategy, 407 Thiobios, 111, 411
Stadler, L. J., 295 Thompson, D., 271, 312, 369371
Starlings, long-billed, 187 Thomson, K., 194, 277, 278
Stasis, 326 Three-ring circus, 5
Stebbins, G. L., 296, 415 Threshold transition, 359
Step mechanisms, 301 Thrombin, 169
Steroids, 231 Thyroxine, 192
St. Hilaire, E. G., 16, 181 Todd, N., 108
St. Hilaire, I., 295 Toleration, physiological, 144
Stiassny, M., and Meyer, A., 416 TRAM systems, 260
Streptomyces, 102 Transcriptional gene silencing by RNA, 230
Stress, 55, 349 Transformation theory, 271
Successful monsters, 368 Transgenesis, 243
Suess, E., 350 Transition function, 312, 344
Sulfur-oxidizing bacteria, 121 Transposable elements, 241244
Sulfur-oxidizing symbiosis, 121, 411 Transposase, 281
Supergenes, 224 Transposition of limb placement, 193
Super-organism, 110 Transposons, 241
Symbiocosms, 99 Triceratops, 276
Index 517
Tridacnidae, 112, 123, 412 Water

Trojan genes, 7 critical point, 351
Tubulins, 170 emergent properties, 115, 374, 375, 427
Turner, J. S., 346, 349 Water ouzel, 321
Turtle carapace, 197 Wax layers, in insects, 150
Tyrannosaurus rex, 210 Weak emergences, 375
Weele, C. van der, 206, 207
Uexkll, J. J. von, 180, 224, 308, 354 Wells, W. C., 261
Ultra-Darwinism, 4, 59, 407, 432 Weng, G., Bhalla, U. S., and Lyengar, R., 163,
Ultramorphosis, 192, 267 347
Ulva, 122 West-Eberhard, M. J., 177, 189, 204
Undulipod, 106 Whale evolution, 210
Uneven crossing over, 237 Wheeler, W. M., 109
Urease, 173 Whewell, W., 129
Uricase, 173 Whitehead, A. N., 299
Uricotelism, 173 Whittaker, R. H., 120
Use-It-Or-Lose-It principle, 250 Wholes greater than sums of their parts, 82,
Uvarov, B., 188 114, 313, 330
Whyte, L. L., 55, 139, 308, 342
Varied repeats of genes, 165, 239, 354 Wigglesworthia glossidinia, 100
Vasopressin, 167 Williams, G. C., 1, 22, 24, 37, 59
Vavilov, A. N., 54 Willmer, E. N., 214
Vegetative repetition, 295 Wilson, E. O., 60, 70, 110, 124, 129
Vendiobionts, 213 Wimsatt W., 14, 70, 290, 303, 316, 341
Venn diagrams, 300, 306 Wnt (wingless), 247
Vernadsky, V., 350 Wolbachia, 100, 243
Vesuvian evolution, 242 Wolff, C., 295
Vie libre, 175 Wollman, Eugene and Elisabeth, 97, 98
Viral transduction, 119 Woodger, J. H., 137, 157, 181
Virchow, R., 128 Wood Jones, F., 209
Vital spark, 318 Wood lice, 113
Vitelline protein, 171 Wright, E. E., 167
Vitellogenesis, 205 Wynne-Edwards, K., 151, 152
Vrba, E., 289, 275, 304 Wynne-Edwards, V. C., 318, 420
Vrba, E., and Eldredge, N., 303
Vrbas rules of emergence, 305 Xenopus laevis, 236
Waagen, W., 268 Y chromosome, 257

Waddington, C. H., 47, 139, 146, 179, 181,
189, 195, 204, 225, 308 Zootermopsis angusticollis, 102
Wake, D., and Roth, B., 199
Waldrop, M., 382
Wallace, A. R., 35, 48, 53, 132

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50904Reid 12/20/06 3:48 AM Page 1

Natural selection is commonly interpreted as the fundamental mechanism of evolution.

Robert G. B. Reid is Emeritus Professor of Biology at the University of Victoria, British

Vienna Series in Theoretical Biology

The MIT Press

Evolution of Communication Systems: A Comparative Approach, edited by D. Kimbrough Oller and

Biological Emergences: Evolution by Natural Experiment, Robert G. B. Reid, 2007

Evolution by Natural Experiment

For information on quantity discounts, email special_sales@mitpress.mit.edu.

Library of Congress Cataloging-in-Publication Data

Reid, Robert G. B., 1939

Introduction: The Re-invention of Natural Selection 1

4 The Physiological Arena 137

5 Development and Evolution 179

6 Epigenetic Mechanisms 223

8 The Re-invention of Emergence 289

9 From the Particular to the General 329

10 An Emergence Theory 363

11 A Biological Synthesis 401

Gerd B. Mller, University of Vienna and KLI

Nobody is going to re-invent natural selection. . . .

The Need for a More Comprehensive Theory

Alas, in every subsequent generation of evolutionists, familiarity has bred contempt as

Are All Changes Adaptive?

In The Variation of Animals in Nature (1936), G. C. Robson and O. W. Richards

The Evolution of Whole Organisms

Because reductionism, whether as a simple bias or as an extreme prejudice, is the

Adaptability is an emergent property of biological wholes. At its point of emergence

The major operation of neo-Darwinist research is measuring the fitness of variants in

proportions, as occurred in the evolution of a giraffe from a short-necked okapi-like

What Are the Options?

The re-invention of natural selection as an obstacle rather than a cause, or simply as a

antithesis. Several evo-devos (developmental evolutionists) are hoping for such a

Breakthrough experiment extends the metaphor. Any invention can be so distinc-

The Rate and the Gait of Evolution

A Generative Emergence Theory

continues to permeate evolutionary writing. Selectionists themselves distinguish

The transitions must be explained in terms of immediate selective advantage to replicators. We

Venturing into unexplained phenomena that most of their fellow ultra-Darwinists

toward higher-order emergences. As an organismal biologist, I take the high road,

would present evolutionary history as a mixture of rapid saltations (progressive and

Mutation is of course, a necessary precondition to continued evolutionary change. So evolution

If natural selection is the filter, whats making the coffee?

The Darwinian Paradigm

persuasively. For Darwin, evolution had to be through modification by natural

Neo-Lamarckism and the Rise of Neo-Darwinism

neo-Darwinist, August Weismann, who had pledged to purge evolutionary theory of

which involves random exchanges of homologous chromosomal material, leading to

Neo-Darwinist Natural Selection

phenomenon is immediately superior. Business entrepreneurs, often social Darwinists,

An interesting contrast is found in the way Ivan Schmalhausen used pressure in

tions of the phenomenon in question. And yet the progressive or complexifying

The Modern Synthesis

Many biological studies had been developed independently of evolutionary theory.

evolutionary debate. However, the reverberating extremism of ultra-Darwinism might

Simply quoting Kuhn is philosophical commentary, and The Structure of Scientific

The Loss of Life, Organism, Mind, and Evolution

Attrition of the Modern Synthesis

The Rule of Gradualism

continuous change. Richard Goldschmidt argued for the saltatory effects of

If a material element, or a combination of a thousand material elements in a molecule are alike

This demonstrates a distinct contrast between Darwinism and emergentism, because

sudden speciation followed by periods of unchanging stasis. Since ontogenic and