70 Chapter 4 Introduction to Metazoa

called peramorphosis (= extended shaping). The narwhal's

enormous tooth is an example of peramorphosis.
Pedomorphosis often t'esults in descendants that are
smaller and anatomically simpler than their ancestors. Small
body size and short generation time (because the develop-
mental program has been truncated) typify many species that
have colonized unpredictable or changeable environments
such as temporary pools, and perhaps the plankton commu-
nity. Pedomorphosis is also common among symbiotic
species, such as certain parasitic barnacles (Fig. 19-83). In
these, the nonpedomorphic female is modified to absorb
nutrients from the host and to produce the myriad eggs and
offspring necessary to infect new hosts. Compared with the
female, the pedomorphic male is a dwarf, little more than
a sexually mature larva, parasitic on the female, whose only
role is to provide sperm to fertilize the female's eggs. Being
tiny, the male does not corn pete substantially with the female
for the host's nutritional resources, allowing her to direct
more food-energy to egg production. Finally, pedomorphic
dscendants of large-bodied ancestors have colonized
entirely new habitats. As shown in Figure 4-10, heterochrony
in a family of segmented worms (polychaetes) enabled the
small-bodied pedomorphic descendant to colonize the
minute water-filled spaces between sand grains (an intersti-
tial community).
Peramorphosis typically results in descendants that are
larger and anatomically more complex than their ancestors.
Much of the story of metazoan evolution, as we have indi-
cated throughout this chapter, is the achievement of large
body size. Large body size and long generation times should
be favored in constant or predictable environments such as
the deep sea, upwelling areas of the sea, and coral reefs.
Other advantages of large body size were discussed earlier in
this chapter.
Throughout this book, we will use the terms pedomorpho-
sis and peramorphosis to describe significant and appropriate
examples of heterochrony. You should be aware, however,
that each of these categories is divided into three subcate-
gories based on the exact form of heterochronic change.
In the worm example, the morphogenesis of a functional go-
stage of the ancestral hfe cycl_e __
that early
_
a normal (ancestral) rate of development with an early onset
of thus-arrestfigTurffi'cieveTOpmerilof1lie
rionrproiutive (somatic) parts of the
I!lal
___ <!_<'_velopmental rate of somatic
structures, .. meaQiiJ,g. t}}at_diffeien tiation of the body lags per-
manently behind reproductive development; or postdisplace-
ment, a normal (ancestral) rate and period of development
with a delayed onset (postponed start of differenciation) of
somatic structures, resulting again in a sexually mature juve-
nile body. These three forms of pedomorphosis and the
similar categories of peramorphosis are summarized in Figure
4-11. Although they are easy to define in theory, these cate-
gories are difficult to distinguish in practice and, for that
reason, we use only the general terms pedo- and peramorpho-
sis in this book.
ORIGIN OF METAZOA
Most zoologists agree that metazoans share a common ances-
try with sorne unicellular organism. The classical colonial
theory, in which Metazoa is derived from a colony of flagel-
lated protozoa, is the most widely accepted hypothesis among
contemporary zoologists (Fig. 4-12). An alternative hypothe-
sis, the syncytial theory, proposes that metazoans evolved
from a multinucleate but unicellular plasmodium similar
to a slime mold or perhaps a ciliate protozoan. Later,
membranes evolved to produce a cell boundary around each
of the nuclei. The syncytial theory receives sorne support
from the development of organisms such as slime molds
or insects (Drosophila), in which an early multinucleated stage
is followed by cellularization to form a multicellular body.
However, phylogenetic analysis based on morphology and
gene sequences as weil as the developmental patterns of most
animais contradict the syncytial theory and favor the colonial
theory. For these reasons, we consider only the colonial
theory here.
A modern version of the colonial theory states that
the premetazoan (a protozoan) consisted of a small spherical
colony bearing a surface layer of flagellated cells that was used
for locomotion and feeding (Fig. 4-12C). The colony origi-
nated from a cell that divided repeatedly by mitosis, but the
daughter cells did not separate after cell division. Those
daughter cells were surrounded and held together by a pro-
teinaceous ECM in which they were deeply embedded. The
gelatinous ECM also occupied much of the interior of the
sphere. Similar to extant choanoflagellates, the cells each bore
a single collared flagellum. A few nonflagellated cells, capable
of giving rise to flagellated cells and gametes, were scattered
in the subsurface ECM (Fig. 4-12C).
Severa! facts support such a flagellate ancestry. Flagel-
lated, or monociliated, collar cells-cells with a single fla-
gellum and collar of microvilli-are widespread in meta-
zoans, and the ciliated cells of lower metazoans, particularly
sponges, jellyfishes, sea anemones, and corals, are exclu-
sively monociliated (Fig. 4-13B). Molecular and morphologi-
cal data both indicate that choanoflagellates and metazoans
are sister taxa. An ECM to which cells are attached and
through which they move is nearly universal in metazoans.
Cellular specializations, such as eggs and sperm, have
evolved in sorne colonial flagellates, such as the spherical,
colonial Volvox.
Although it is unrelated to metazoans, Volvox is an analog
for an ancestral metazoan because it demonstrates how a mul-
ticellular organism evolved from a unicellular ancestor, in this
case a Chlamydomonas-like cell. Volvox is not the ancestor of
Metazoa, but rather is an autotrophic organism with plantlike
cells. rRNA sequence data indicate that multicellularity in
Volvox evolved 50 to 75 million years ago, far too late for it to
have been a progenitor of metazoans, which had their origin
at !east 600 million years in the past. Thus, the volvocids
evolved multicellularity in parallel with the metazoans (and
with at !east four other groups: fungi, brown algae, red algae,
and green plants).
FROM THE BOOK: INVERTEBRATE ZOOLOGY: A FUNCTIONAL
EVOLUTIONARY APPROACH (RUPPERT, FOX, BARNES)
ECM - EXTRACELLULAR MATRIX
8
Ameboid
ce li
Ameboid cell
C Hypothetical premetazoan
Evolutionary Origins 71
External ecm
D Hypothetical protometazoan
Ante ri or
pole
FIGURE 4-12 Origin of Metazoa: choanoflagellate colonies and metazoan evolution. A and B. different forms
of the choanoflagellate colony Proterospongia haeckeli. C, A hypothetical premetazoan based on the
choanoflagellates in A and B. 0, A hypothetical protometazoan showing cellular specialization along an
anterior-posterior axis. Surface cells are bou nd together and in mutual contact, thus allowing physiological
regulation of the interior of the body.
The actual sister taxon of Metazoa is most likely
Choanoflagellata. Among the. extant choanoflagellates,
colonies of Proterospongia haeckeli (Fig. 4-12A,B) closely
resemble the hypothetical premetazoan (Fig. 4-12C). The
colony consists of flagellated collar cells embedded in
the surface of a gelatinous ECM. Cells undergoing division
and lacking flagella occur deeper in the ECM (Fig. 4-12B).
A surface sheetlike layer of cells and an ECM containing
individual free cells foreshadow the two primary metazoan
tissues, epiti).elial and connective, described earlier in this
chapter. At the cellular leve!, choanoflagellate collar cells
are virtually.identical to collar cells (choanocytes) found in
the metazoan sponges. A choanoflagellate cell and sponge
choanocyte both have a single flagellum surrounded by
a collar of microvilli and a flagellar shaft with a bilateral
vane (Fig. 4-13). In both, the flagellum is anchored
10
the cell by microtubules, which radiate from the flagellar
basal body.
.The hypothetical first metazoan, the protometazoan
(Fig. 4-12D), may have differed from the premetazoan (Fig.
4
-12C) in severa! ways. First, the surface cells probably
adjoined or were in contact with each other, thus
faCihtating intercellular communication and providing a
barrier between the external environment and
e ECM in th!! interior of the body. Second, the close
associati f
b on o adJacent cells largely excluded the ECM from
the cells, thus separating the ECM into external
pe ;nternal layers, each of which could then adopt inde-
n ent functions (Fig. 4-12D). Third, the body was polar-
ized along the anterior-posterior axis. Fourth, the separation
of layers and body polarity promoted cell specialization
(Fig. 4-12D).
ORIGIN OF POLARITY AND
CELL SPECIALIZATION
Most motile protozoans are polarized cells that have leading
(anterior) and trailing (posterior) ends or, if sessile and
attached, they have oral free ends and aboral attached ends.
Metazoans are similarly polarized, depending on whether they
are motile or sessile, but how did the polarity of the multicellu-
lar metazoan body evolve from the unicellular polarity of pro-
tozoans? A clue to the answer is found in the eggs of severa!
groups of metazoans. During oogenesis in these groups, the
eggs express a rudimentary flagellum and a collar of microvilli
at a site on the cell surface that corresponds to the animal pole
ofthe zygote (Fig. 4-13B-D). In certain invertebrate taxa, the
animal pole corresponds to the anterior end of the larva
(although it is the posterior end in others). Additional
research is needed, but the current evidence suggests a line of
descent from the polarity of a choanocyte to the primary ante-
rior-posterior polarity of the metazoan body (Fig. 4-13).
The protometazoan probably was polarized along an
anterior-posterior axis, but what environmental conditions
might have selected for the evolution of such polarity? For an
aquatic metazoan, the environment presents itself in gradients
of light, temperature, oxygen, and food availability. If, for
72 Chapter 4 Introduction to Metazoa
Tail
E
Head
8
A
Anterior Animal
De
l Veget
Effective stroke ! ::-.
..
: ...
/ c : .. ;::-
Va ne
Radial
microtubule
anchor
FIGURE 4-13 Origin of metazoan polarity. A. Primitive coll ar ce li with
a flagellar va ne, as occurs in protozoan choanoflagellates and metazoan
sponges. B, Choanocyte-like monociliated cell from the surface epithelium
(epidermis) of an anemone larva (Cnidaria), showing its power stroke in
the direction of the accessory centriole. C. Early oocyte of a sea cucumber
(Echinodermata) showing a low collar and rudimentary cilium; 0, Sea
cucumber zygote in the sa me orientation as the oocyte in C. Note th at the
animal and vegetal poles correspond to the apex and base, respectively,
of the epithelial cell in B. E, A typical metazoan sperm showing its
polarity in relation to an epithelial spermatogonium from which it rose.
F, Anterior end of a simple larva (Cnidaria). Note the position of the
accessory centrioles, which indicate posteriorly directed.ciliary effective
strokes and thus forward movement in an anterior direction. (B, Modifod
and redraum from lUeger, R M. 1976. Monociliated epidermal cells in
Gastrotricha: Signijicance for concepts of early meto.wan evolution. Z. z.ooL Syst.
Evolut.fursch. 14:198-226; C-E, ModifodfromFrick,J E., andRuppert, E. E.
19%. Primordial germ cells of Synaptula hydriformis (Holothuroitka:
&hinodermata) are epethelial flagellatedrcollar cells: Their apica/rbasal poimity
becOTMS primary egg polarity. Biol Bull. 191:168-177, and Frick, J E., and
Ruppert, E. E. 1997. Primordial germ cells and oocytes of Branchiostoma
virginiae (Cephaloclumlata, Acrania) are jlagellated epithelial cells: Relationship
between epitMlial and primary eggpolarity. Zygote 5:139-151.)
example, the availability offood is related to light (through pho-
tosynthesis), natural selection would favor any variant inclividual
capable of detecting and following a light gradient. This is best
accomplished with a clirection-sensitive sensory capability cou-
pied with a directional (polarized) locomotory system. Thus,
selection may have favored any organism capable of tracking a
resource concentration graclient. Altematively, developmentai
biologist Lewis Wolpert suggests that body polarity evolved from
attachment to a Attachment to a rock in water, for
example, places an organism at an interface, a very steep gradi.
ent. Once attached, variants would be favored that adhere well
at the attached end and perform other tasks, such as feeding, at
the opposite end. This again leads to a polarized body.
Once polarity was established, movement would create an
environmental graclient along the locomotory axis that would
favor differentiai expression of traits (Fig. 4-120). For exam-
ple, enhanced membrane sensitivity to environmental stimuli
might be favored in cells at the anterior end of the body
because they are the first to encounter changes in environ-
mental conclitions. Similarly, enhanced flagellar growth,
density, or activity might be favored in cells at the equator, or
widest part of the body, since those locations best contribute
to locomotion. Cells with a capacity for division, leading to
growth, might be favored at the. posterlor end, because in that
position they contribute to and interfere !east with locomo-
tion. Thus, motility along a polar axis may itself promote
cellular specialization because the cells occupy different fixed
positions in an environmental graclient (Fig. 4-120).
According to a hypothesis by developmental biologist Leo
Buss, the origin of rnetazoan cell specialization may be
related to a conflict between the demands for growth and
locomotion. Volvox, Proterospongia, and planktonic blastula
stages of metazoans require flagellated surface cells for loco-
motion, but most flagellated cells cannat divide by mitosis be-
cause the centrioles needed to form the mitotic spindles are
already in use as the flagellar basal bodies. A metazoan flagel-
lated cell can divide only after the flagellum regresses and its
basal bodies are freed to form the mitotic apparatus. Th us, the
options for growth in a premetazoan composed solely of fla-
gellated cells (for example, the species of Proterospongia in Fig.
4-12A) are: (1) enlargement of existing cells; (2) disassembly
of flagella, cell clivision, and then flagellar reassembly; (3) clivi-
sion of a few cells scattered throughout the embryo while ath-
ers retain flagella; or ( 4) division of a few localized cells set
aside for growth (Fig. 4-12B-O). Option 1, because of the
restricted number of cells, limits ultimate body size, although
Volvox daughter colonies and a few postembryonic micrometa-
zoans grow by cell enlargement only. Option 2, by requiring
the regression of flagella, compromises locomotion. Options 3
and 4 both permit growth and locomotion, but most inverte-
brate metazoans have adopted option 4. The setting aside of
mitotically active cells enables metazoan growth without
compromising locomotion (Fig. 4-12B-O). (A related evolu-
tionary event was the setting aside of germ cells capable of
meiosis.)
Surface flagella are a functional necessity for locomotion in
the protometazoan, but what is the optimal position for the
set-aside growth cells? Buss suggests that placement at the
surface might have resulted in overgrowth of locomotory cells
or growth of a tumorlike appendage, either of which would
negatively affect motility. Intemalizing the growth cells,
however, would neither distort the body surface nor inteffere
with the locomotory cells. Perhaps for these reasons the
protometazoan did intemalize its growth cells and the process
was preserved, as gastrulation, in its descendants (Fig. 4-14;
.ii

j
j
1
Blastocoel
(ECM)
NOGROWTH
Evolutionary Origins 7;
Monociliated cells
(epithelium)
lnternalized ceii}Connective
ECM tissue
lngressing cell
Egg

___ ........;._ GROWTH
FIGURE 4-14 Origin of cel! and tissue specialization: segregation patterns of growth cells in hypothetical
protometazoans. A. Blastula-like developmental stage of a hypothetical organism; 8, Hypothetical blastula-like
organism that does not grow because its cells retain locomotory cilia and thus cannot divide by mitosis. C-E,
Growth by internalizing nonflagellated mitotically active cells in three simple hypothetical metazoans. The
patterns in C-E a Iso represent three basic forms of gastrulation in actual animais. c. multipolar ingression; D.
unipolar ingression; E, invagination (or emboly). Note how the embryonic blastocoel (ECM) is equivalent to adult
connective tissue. (Based on ideas in Buss, L. W 1987. The Evolution of lndividuality. Princeton University Press,
Princeton, NJ 201 pp.)
also see Reproduction and Development in chapter). An
intemalization of cells capable of mitosis also evolved in Volvox
and Proterospongia haeckeli (Fig. 4-12B). A colony of P. haeckeli
grows by the addition of new surface choanocytes that origi-
nate by mitosis of cells in the subsurface gel. Similarly,
colonies of Volvox consist of a thousand or more flagellated
surface cells and invaginated subsurface pockets of nonflagel-
dividing cells (gonidia). The gonidia can give rise to
either new colonies or germ cells.
. The simultaneous requirement for locomotion and growth
10
early metazoans favored a body with two layers of differenti-
ated cells (Fig. 4-12D). The layering of cells established tissues
(as described earlier in Cells, Tissues, and Skeletons) and an
exterior-interior gradient. The surface cells bad direct access
to and other raw materials, but were constfained by the
reqUirements for locomotion and for interfacing with the
environment. The in teri or cells, liberated from direct
:teraction with the environment, became specialized for
a production, nutrient storage, and, with the evolution of
gut, the digestion offood.
ORIGIN OF COMPLEXITY
Evidence supports the hypothesis that metazoans evolved
from protozoan colonies in which initially similar cells
became specialized for different functions. If so, the evolu-
tion of Metazoa can be described as a replication of similar
units (cells) followed by unit specialization and integration
into an organism at a new, higher level of complexity.
This replication-specialization-integration of units. sequence
is a general pattern in the evolution of large body size and
complexity. An example, as we have seen already, is the
replication, specialization, and integration of cilia on the
body of many ciliates, which are among the largest, most
diverse, most active, and most complex protozoan cells.
Among metazoans, one example is a body corriposed of a
series of similar segments, as in earthworms or crustaceans.
Later, these segments become specialized and integrated
into regions, such as the head, thorax, and abdomen. Exam-
ples at ali levels of biological complexity are illustrated nd
described in Figure 4-15.