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HANDICAP
PRINCIPLE
THE
HANDICAP
PRINCIPLE
A Missing Piece of Darwin's Puzzle
1 3 5 7 9 1 0 8 6 42
Printed in the United States of America
on acid-fre e pape r
Illustrations by Amir Balaban
CONTENTS
Acknowledgments xi
I N T R O D U C T I O N TH E GAZELLE, TH E WOLF, AN D TH E PEACOCK'S TAIL xiii
P A R T I PARTNER S I N COMMUNICATION
C H A P T E R 1 PREY-PREDATO R INTERACTION S 3
CONTENTS
VI
The conflic t inheren t i n courtship . Courtshi p handicap s an d th e infor mation the y convey : feeding ability , superterritories , courtshi p vocaliza tion, colors , scent s (pheromones) , artifact s an d constructions , com binations of signals, long tails, movements an d dances. Leks: congregating
for display . Polymorphic specie s and male s tha t mimi c females. Fisher' s
model o f th e Runawa y Process compare d wit h th e Handica p Principle .
Utilitarian selectio n an d signa l selection .
P A R T I I METHOD S O F COMMUNICATIO N
CHAPTER4
Difficult movements . Ritual fighting. Ritualization: does i t reduce th e information conveyed ? How a ritualized signa l evolves.
CHAPTER6
VOCALIZATION S 6
The correlatio n o f voice with postur e an d tension . Th e information con veyed b y vocal signals . Animal vocabularies: th e connectio n betwee n th e
message and its vocal pattern. Rhythm. Vocal patterns used ove r distance.
Why shout ? Th e duratio n o f vocalization: request s an d commands . Dialogues an d their significance . Mimicry. Do animal s have verbal language?
CHAPTER7
Long tails : are they signals ? Bristling hair o r feathers : an illusio n o f size,
or a handicap? Mane s an d crests . Handicap s tha t interfer e with vision .
Body parts that emphasize the direction o f gaze. Body parts that handica p
Contents
VII
fighting. Can body parts evolve to reduce the cost of signals? The evolution
of horns an d antlers . Signal selection an d th e evolutio n o f feathers.
C H A P T E R 8 TH E USE OF COLO R FOR SHOWING OFF 9
Black in the desert. Black and white in open spaces . Colors in forests and
on cora l reefs. The us e of two colors. Gloss y colors an d movement . Exceptions t o the rules .
C H A P T E R 9 CHEMICA L COMMUNICATION S 1O
Pheromones i n butterflies and moths: chemical handicaps. Yeast sex pheromones an d propheromones : th e rol e o f glycoproteins . Chemica l com munication within the multicellular body.
P A R T II I TH E HANDICA P PRINCIPLE I N SOCIA L SYSTEM S
C H A P T E R 1 0 TESTIN G T H E BOND 1 1
Territories, groups , and nonterritorial individuals . Rank, avoidance of incest, an d th e lif e strateg y of male s an d o f females . Th e compositio n o f
groups; coalition s o f males and o f females. Struggles without aggressio n
(well, almost). Theories tha t explain altruism : group-selection theor y and
its failings. The theor y of reciprocal altruis m and th e problem of enforcement. Competition over altruistic acts in babblers: sentinel activities, feeding of nestlings, feedin g of other adults (allofeeding), mobbing. Altruism
as a substitute fo r threats. Rank and prestige. "Shyness " ove r copulatio n
as a test of male prestige. Reasons for and consequences of living in groups.
Prestige an d the evolutio n o f altruism: altruism as a handicap.
C H A P T E R 1 3 TH E SOCIAL INSECTS : WH Y HEL P TH E QUEEN? 15
The evolution of social structures in the social insects: conditions that favor
collaboration: foo d storage and helpless offspring; the haplodiploid mech-
viii C O N T E N T
The life cycle of cellular slime molds. Forming the stalk: altruistic suicide?
The individua l selection hypothesis . DIF a s a poison. The differenc e be tween prestalk and prespore amebas . Some remaining questions. When is
a chemical a signal?
C H A P T E R 1 6 PARASIT E AN D HOS T 18
An arms race or a state of equilibrium? European cuckoo s and reed warblers. Grea t spotte d cuckoo s an d crows . The prestige model. Th e Mafi a
model. Acceptin g a parasit e t o minimiz e damage . Neuterin g th e host .
From parasit e to collaborator . Th e less virulent parasite as a collaborato r
against it s virulent variant. The implication s o f assuming a state of equilibrium.
C H A P T E R 1 7 INFORMATIO N CENTER S 1 9
Food sources and social organization: the white wagtail. Communal roosts
as information centers . Insurance agains t evi l days : winter gathering s o f
rooks. Flock s an d loners : the communa l roos t o f kites i n Coto Donana.
Bright adult s an d dul l youngsters: handicaps in food squabbles. How information repositorie s work . Huma n gatherings . Communa l display s at
gatherings: promoting the roost or mutual testing?
P A R T I V HUMAN S
CHAPTER 1
8 HUMAN
S 2O
Contents
IX
red cheek s an d lips; menstruation; breasts and body fat; clothing. Testin g
the huma n socia l bond: the huma n sexua l act as a test o f the bond, self endangerment i n humans : suicid e a s a cr y fo r help . Huma n language :
communication withou t reliability . Decoration , esthetics , an d th e evolu tion of art. Altruism and mora l behavior.
Epilogue 229
Notes 231
Bibliography 245
List of Figures 261
Index 267
ACKNOWLEDGMENTS
ur daughter s Naam a and Tirza took par t fro m th e very beginning i n the
discussions fro m whic h ou r idea s emerged , an d thei r suggestion s hav e
helped us present those ideas here. Naama's presence in these discussions,
and tha t o f her husban d Melvi n Patric k El y in late r years , equipped th e tw o of
them, workin g fro m ou r origina l Hebrew text , t o writ e the versio n o f this book
that now appears in English and other languages. We also thank Amir Balaban for
the skil l and artistr y he brought t o the task of illustrating the book .
Azaria Alo n encourage d an d helpe d u s throughout , bu t especiall y wit h th e
difficult earl y steps . W e wis h t o than k Daniel a Atzmony , Helen a Cronin , Pau l
Eckman, Michal Gil, Jehoshua Kugler , Arnon Lotem, Jonathan Wright , Mina Yarom, Yoram Yom-Tov, and Zohar Zuk-Rimon for reading and commenting on the
whole manuscrip t o r on som e of its chapters .
The first drafts of this book were written well over ten years ago. It is impossible
for u s to acknowledg e al l our friends , students , an d colleague s who rea d some of
these drafts an d made important comment s and suggestions for improvements, or
those wh o provide d photograph s o r videocassettes , o n which Ami r Balaban has
based som e of his lively drawings . W e d o hope that these friends wil l forgive u s
for no t mentionin g al l of them b y name.
xii A C K N O W L E D G M E N T
We thank the staf f o f Oxford University Press, especially our edito r Kirk Jensen, ou r productio n edito r Kimberl y Torre-Tasso, an d ou r devote d copyeditor ,
Nora Cavin. We gratefull y acknowledg e the effort s o f our literar y agent, Richard
Balkin.
Special thanks ar e due to the man y volunteers and students wh o helped with
our field observations of the babblers , gettin g to know these cooperativel y living
birds individually and recording data about their behavior. But above all we thank
the Societ y for th e Protection o f Nature in Israel (SPNI) for allowing all of us t o
live and work in its Field Stud y Center a t Hatzeva.
The income from th e Hebrew editio n of this book is dedicated to a fund which
will b e use d t o continu e ou r stud y of th e babbler s an d t o maintai n the Sheza f
Nature Reserve , where these bird s ca n continue t o live , protected fro m th e up heavals created by modern life. We hope that the English version and other translations of this book will widen th e circl e of friends of the Sheza f Nature Reserve
and its babblers.
Amotz and Avishag Zahavi
I N T R O D U C T I O N
xiv I N T R O D U C T I O
seen it ; by "wasting " time and b y jumping high i n th e ai r rather tha n boundin g
away, it demonstrates i n a reliable way that it is able to outrun th e wolf. The wolf ,
upon learnin g tha t i t has lost it s chanc e to surpris e its prey, and tha t thi s gazelle
is i n tip-to p physica l shape , ma y decid e t o mov e o n t o anothe r area ; o r i t may
decide to look for more promisin g prey.
Even partie s i n the mos t adversaria l relationships, suc h a s prey an d predator ,
may communicate , provide d tha t the y have a common interest : in this case , both
want to avoi d a pointless chase . The gazelle tries to convince the wolf that it is not
the eas y prey the wolf is looking for , and that the wolf would be wasting time and
energy by chasin g it. Even i f the gazell e is sure that i t ca n outrun th e wolf , i t to o
would prefe r to avoid an exhausting chase. But in order t o convince the wolf no t
to give chase, the gazelle has to expend preciou s tim e and energy that i t will need
should th e wol f ignore its signals and decid e t o chas e it anyway .
The encounter betwee n th e gazelle and the wolf dramatize s the basic theme of
this book: in order to be effective, signal s have to be reliable; in order to be reliable ,
signals have to be costly .
The hig h cos t tha t animal signaling often involve s is clearly seen in the cas e of
the peacock . Mos t peopl e hav e seen an d admire d a peacock, spreadin g an d quivering his enormous taila fan of glistening feathers, adorned with blue and green
"eyes." But to be abl e t o put o n such shows , peacocks hav e to drag massive tails
around mos t o f the year . By managing to fin d foo d an d avoi d predator s despit e
such a burden, a peacock prove s tha t he is the high-qualit y mate that th e peahe n
is seeking to fathe r her futur e chicks .
This i s another basi c them e o f our book: tha t
there i s a logica l relationshi p betwee n th e signa l
and th e messag e i t conveys . Th e gazell e display s
its confidence in its ability to outrun th e predato r
by drawin g attentio n t o itsel f an d b y expendin g
precious tim e an d energ y that i t will need shoul d
its signal not be heeded. The peacock proves his
strength and agility by carrying a heavy load, as
does a stag carryin g heav y antlers . Eac h signa l is
closely related to its message. A perso n ca n signal courage by courting danger , for
example, bu t courtin g dange r doe s no t attes t t o wealthwhic h ma y be demon strated b y wasting money.
The investmen t that animal s make in signal s is similar to the "handicaps " imposed o n th e stronge r contestant s in a game or a sporting event : for example, th e
removal of the superior player's queen in a chess match, the extra weight the swifte r
race horse mus t carry , or the scor e o f several strokes tha t the more accomplishe d
golfer start s with. A handica p prove s beyon d a doubt tha t th e victor's wi n is due
to mastery , no t chance . Th e peacock' s tai l an d th e stag' s antler s ar e no t mer e
disabilities; rather , the y ar e handicap s i n thi s ver y specia l sense : the y allo w a n
individual animal to demonstrat e it s quality.
Introduction x
Are animal signals always reliable? We believe that most signals are: before an
individual acts on information it receives through signal s from anothe r individual ,
it first needs to chec k the reliability of that information. We suggest a very simple
principle: if a given signal requires the signaler t o invest more in the signal than it
would gai n by conveyin g phony information, then fakin g i s unprofitable an d th e
signal is therefore credible. I f a gazelle that is slow or weak sends the wolf a phony
signal about its speed and strength by stotting, it wastes what little strength it has
on puny jumps that will only convince th e wolf that it is easy prey. Such a gazelle
would d o better t o fle e fo r its life an d hope fo r the best . T o gauge the reliabilit y
of a signal , then , on e ha s t o conside r th e investmen t i t entails . Th e costth e
handicap tha t th e signale r take s onguarantees that th e signal is reliable.
When w e first suggested this Handica p Princi ple i n 1975 l i t wa s almos t unanimousl y rejected.
Many papers were published using formal, explicit
mathematical models "proving " tha t the Handica p
Principle doe s not work,2 or that it might apply only
under ver y special conditions. 3 Thi s trend change d
in 199 0 whe n Ala n Grafe n publishe d two papers 4
using differen t mathematica l models t o sho w tha t
the Handicap Principle i s generally applicable, an d
that it is a sound principle that can ensure reliability
in communicatio n betwee n competin g organisms .
Since then , th e Handica p Principl e ha s becom e
widely accepted. 3
Throughout al l these years , while our colleague s were debating th e validity of
the principle , w e continued t o observ e an d explor e th e livin g world aroun d us .
The Handicap Principl e reveale d to us an endless arra y of new ways to understand
such phenomena as the extreme expenditures often involve d i n sexual advertise ment, th e evolutionar y enigma of anima l altruism , an d th e working s o f collabo rative systems in the animal kingdom, which could not easily be explained in terms
of straightforward , utilitarian natura l selection .
Our investigation s into the ramifications of the Handicap Principl e coincide d
with ou r studie s o f the babblers, group-livin g songbirds, at Hatzeva in the Arava
Valley of southern Israel . W e have been studyin g these small desert birds fo r th e
last twenty-fiv e years. The y ar e used to ou r presence ; we often ge t within a few
feet or even inches of them. As far as they are concerned, we are not much differen t
from the herds of goats and camels with which they share the desert. We can watch
them very closely, observe the fine details o f their behavior, an d hear the soft an d
subde vocalizations wit h which they communicate with one another. We can identify eac h individual bird b y the colore d le g bands w e put o n it s legs when it was
a nestling.
All members o f a babbler grou p participat e i n th e defens e of thei r territor y
and i n the car e of nestlings, eve n when the nestling s ar e not thei r ow n offspring .
XVI I N T R O D U C T I O
The birds perform many other altruistic acts, such as feeding other adult member s
of thei r grou p an d standin g guar d whil e th e res t o f th e grou p i s feeding. Such
activities are difficul t fo r researcher s o f evolution t o explain. We discovere d tha t
these altruisti c behavior s serv e to advertis e each babbler . I n othe r words , each
babbler's investment in altruistic acts demonstrates the validity of its claim to social
statusto prestige. We learned from babblers how important it is to animal s t o
be able to measure the strength of social bonds; that need explained the babblers '
group "dances," and their clumping together to rest. The Handicap Principl e also
explains th e birds ' shynes s abou t se x an d eve n th e detail s o f thei r ver y subtl e
decorative markings.
We did not start out seeking a unifying principle i n biological communication .
All we attempted t o d o a t first, in 1973 , was to explai n the evolutio n o f the peacock's tail to a student an d colleague , Yoa v Sagi , whofo r goo d reason , a s it
turned outcoul d no t see the logic in Fisher's runawa y process, then the current
theory. Ou r broa d applicatio n o f the Handica p Principl e develope d slowly : one
finding led to another, until we realized we were dealing with a general principle .
Many people, includin g those who now accept th e Handica p Principle , have
not ye t attempted to appl y i t broadly to biological signaling . W e think tha t th e
explanations an d models we present i n this book ar e more plausible, an d fit the
known facts better, than those commonly found in textbooks. We expect our ideas
to serv e a s a starting point fo r mor e detaile d studie s an d experiments . Som e of
our explanations will prove valid as they stand; in other cases, reality will turn out
to be even more fascinating and complex than we now imagine. We hope that this
book wil l encourag e th e searc h fo r reliabilit y and fo r it s unavoidabl e cos t i n all
systems of biological signaling. W e believe that this search wil l change our under standing of the natura l world in a myriad of ways.
P A R T1
PARTNERS I N
COMMUNICATION
C H A P T E R1
PREY-PREDATOR
INTERACTIONS
4 PARTNER
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considerable distance . In fact, when we try to find babblers in their vast territories,
which often cove r more than a square kilometer, we have a good chance of missing
them whe n the y feed quietl y amon g the bushes; bu t a s soon a s we see a raptor in
the distanc e we stop the ca r and listen fo r barking babblers. Th e sharp barks th e
birds emi t periodicall y a s long a s a raptor i s around allo w usand probably th e
raptorto locate th e group. The call s seem to serve the interests o f the predato r
rather than the group .
One coul d possibl y understan d th e first bark a s a warning to th e group , an d
perhaps th e secon d an d th e thir d a s effort s t o mak e al l members o f th e grou p
aware of the danger . But wha t is the poin t o f repeating th e call s afte r th e entir e
group ha s already taken cover ? And who m ar e they "warning," when th e entir e
group joins the sentine l a t the top o f the canopy, barking together ?
And if the bar k is a warning to th e res t of the group ,
why i s i t s o loud ? Babbler s ofte n vocaliz e softl y whil e
feeding, bu t th e "warnin g calls " ar e hundred s o f time s
louder tha n thes e sound s an d ma y be hear d ove r hal f a
mile away. Why do babblers rais e the volume of their calls
to a level that ca n alert a predator to their presence pre cisely when a predator i s in th e areaan d befor e i t ha s
had a chance to notice th e well-camouflaged group?
There is also a theoretical difficult y regardin g the evolution o f warning calls. For a traitsuch as the tendency
to call out when one spots a predatorto spread through
a population b y natural selection, that trait has to improve
the chance s tha t th e specifi c individua l wh o possesses it
will survive and pass it on to descendants. Bu t the investment in so-called warning
calls is made by the callers , while the benefit goes to the listeners. 1
Indeed, caller s an d listener s ar e no t eve n necessaril y of th e sam e species : a t
Hatzeva, where we observe, the babblers, shrikes , blackstarts, bulbuls, and wheatears also call out loudly at the appearanc e of raptors. Some of these birds, such as
shrikes in winter, ar e solitary and have no collaborato r t o warn, not eve n a mate.
The fac t tha t th e barks tell anybod y who happens t o be around , including othe r
bird speciesan d for that matter, including ustha t there i s a raptor i n the sky
does not mean that they evolved for that purpose. S o we searched for an alternative
explanation.
Loud call s mak e sens e whe n th e listene r i s distant. 2 Sinc e th e rapto r i s fa r
away fro m th e sentinel , i s i t possibl e tha t th e intende d listene r i s actuall y th e
raptor? Th e notio n make s eve n mor e sens e i n view of the callers ' behavio r afte r
a rapto r lands : th e babbler s ofte n approac h th e predato r an d "mob " it . On e
does not hea r an y clear separatio n betwee n th e warnin g call s an d th e mobbin g
calls: on e behavio r merge s into th e other . I t i s widely accepte d tha t mobbin g i s
directed a t the predator 3; is it possible tha t the "warning " call s ar e also directe d
at it ?
Prey-Predator Interactions 5
Communication requires cooperation. There is no point in talking unless someone is listening, and there is no point i n listening unless it might be to the listener's
advantage to do so. These two conditions ar e met only if there is a common interest
between th e parties . Wha t ca n be th e commo n interes t betwee n a rapto r an d a
babbler?
A rapto r ca n catc h a babbler onl y b y surprise, o r whe n th e babble r i s far fro m cover .
Babblers ar e masters of the thickets. Inside th e
vegetation, thei r stron g feet , lon g tails , an d
short wines enable the m t6o dodee and outma,T
.
,
neuver an y predator.
I t i s not unusua l to se e a
group o f babblers hoppin g an d callin g loudl y
in a bush o r a tree that a raptor has perched in.
Indeed, at every loud noise, suspicious movement, or urgent warning call, babblers
hurry into a thicket, where a predator ha s no chance against them; a predator tha t
knows i t has been see n b y babblers i s wasting its time if it stay s in the area . And
as long as the predator remain s in the vicinity, the babblers have to stay near bushes
and track the raptor's movements to make sure it does not catc h them by surprise.
If th e babbler s notif y th e rapto r tha t the y hav e see n it , bot h partie s gain . Th e
raptor move s o n t o anothe r feedin g ground , t o tr y an d surpris e other prey ; th e
babblers ca n resum e thei r feeding . I t make s sens e fo r th e babbler s t o signa l t o
the raptor, and for the rapto r to pay attention t o their signal.
But on e coul d argu e that onc e th e raptor s hav e learnedor evolved th e abilityto pa y attentio n t o th e "warnin g calls, " babbler s coul d "cheat, " emittin g
warning barks periodically, whether o r not they see a raptor. The raptor, however,
has a defense agains t such trickery : it put s th e burde n o f proof o n th e babblers ,
reacting to call s only when it is sure that they are directed a t it individually.
The behavior o f the "warning" babble r fits this hypothesis: the babbler climb s
to th e to p o f the tre e t o bark, eve n though i t could hav e watched th e rapto r and
called fro m withi n th e canopya s i t doe s when i t i s really frightened . The bir d
barks, disclosin g it s location, rathe r tha n trilling , a s babblers d o under othe r circumstances, and which makes them much more difficult t o locate.4 A babbler who
would chea t by going to the to p o f the canop y and barking before it actually saw
a predator woul d expose itself to raptors it might not have noticed. That risk helps
ensure that if a babbler goe s to the top o f the tree and declares it has seen a raptor,
it has indeed see n one.
If th e rapto r lands , th e babbler s ofte n approac h i t an d mo b it , erasin g an y
doubt th e rapto r ma y have tha t i t i s indee d th e objec t o f thei r calls . Th e call s
change fro m bark s t o trills , interrupte d b y tzwicks wheneve r th e rapto r moves ,
which proves that the babblers ar e in fact watching it continuously. Bulbuls, blackstarts, sunbirds , warblers , an d wheatears al l join th e gathering , so the rapto r ca n
see tha t the y to o ar e awar e o f it s presence . B y taking th e calculate d ris k o f ap proaching th e predator, th e birds increas e the reliabilit y o f the message, which is
PARTNERS I N COMMUNICATIO N
that the predato r ha s no chanc e of catching them. Indeed, they may even expose
the raptor to its own enemies, such as bigger predators or humans, who may notice
the commotion and come to investigate .
Having los t th e chanc e t o catc h it s prey by surprise an d itsel f expose d t o risk , th e rapto r i s per suaded t o leav e the area . Bu t mobbing expose s th e
babblers a s well: SordaP collecte d evidenc e showing
that mobbin g bird s ar e occasionall y caugh t b y th e
raptors they mob. This ris k is the price birds have to
pay to convince the raptor that they are indeed aware
of its presence. 6
Unfortunately we cannot collect dat a on whether
the behavio r o f th e babbler s encourage s raptor s t o
move on. Although the babbler s ar e used t o u s and
do no t min d ou r movin g amon g them , th e raptor s
certainly d o mind, an d our presence causes them to
move away.
Prey-Predator Interactions 7
is guaranteed to be reliable. The wolf avoids exhausting itself in pursuit of a gazelle
it cannot catc h and saves its energy for a more promising chase; likewise the gazell e
will hav e th e strengt h t o fle e fro m a predato r wh o ma y fee l u p t o th e tas k of
overtaking it.
Since 1977 , whe n w e firs t publishe d th e
idea that stotting and "warning" vocalization s
are i n fac t directe d a t predators, 8 zoologist s
have collected som e evidenc e t o suppor t th e
hypothesis that individual prey benefit by signaling t o predators . Fitzgibbo n an d Fan shawe9 collecte d dat a i n th e 1980 s i n th e
Serengeti t o test thi s hypothesis. Fro m a hilltop, they watched th e hunting strategies o f spotte d hyena s and o f hunting dogs , wh o catc h thei r pre y by runnin g i t
down i n a lengthy chase, rather than hunting by surprise, like cheetah s and lions.
Some gazelle s stotte d repeatedl y whe n dog s o r hyena s approached, while other s
did not attempt to stot but rathe r fled right away. Both spotted hyena s and hunting
dogs wen t afte r gazelle s tha t di d no t stot , o r stotte d onl y a little; the y avoide d
chasing those who gav e an impressive display of stotting before their escape. Thus
it seems that predators d o indeed observ e stotting in order to estimate an individual's abilit y to flee.
Hasson an d hi s colleagues 10 collecte d evidenc e o f simila r behavio r i n zebra tailed lizards . When a lizard i s surprised i n th e ope n i t run s awa y a t to p speed .
But when i t is near its hole o r near a bush wher e it is able to hide, it does not flee
but instea d stops an d moves its conspicuous tail from sid e to side. The model they
used t o explai n th e behavio r o f th e lizar d was th e on e w e use d t o explai n th e
behavior o f the babbler s an d the gazelles. 11
We were no t th e firs t t o sugges t tha t potentia l pre y may communicate with
predators. Smythe 12 observed the behavior o f maraslarge Patagonian rodents
when the y meet humans. He realize d that their behavior wa s analogous to that of
stotting gazelles; but maras are solitary, and so he could not interpret that behavior
as a warning t o other members o f their species. Smythe concluded that the fleeing
maras signal to predatorsthat the former manipulate the latter, "inviting" pursuit
only when they are ready for it.
Smythe believe d tha t predator s wer e stimulate d t o pursu e fleeing prey eve n
when the y stoo d t o los e b y doin g so . It di d no t occu r t o Smyth e that pre y an d
predators may have a common interest . He wa s aware o f the shortcoming s o f his
explanation; he suggested that evolution was not yet complete, an d that eventually
the predator s migh t evolve the abilit y to ignore such temptations. Bu t any feature
whose benefits we do not understan d ca n be dismisse d by saying it is not ye t well
adapted an d will change in the future . W e thin k it more likely that most feature s
are well adapted and in equilibrium with their environment; experience has shown
us that thi s approac h produce s bette r explanations . Eve n when on e has no ready
explanation fo r a given phenomenon, i t is best t o assum e that we are still missing
partners in communication
Prey-Predator Interactions 9
vocalizations in order t o asses s the abilit y of the runne r t o flee. Both th e pursue r
and th e pursued gai n from communicating .
Once again we have drawn a parallel between the behavior of animals and that
of humans. Some deride suc h comparisons as "anthropomorphisms" an d conside r
them "unscientific. " Bu t a model i s a tool; and anthropomorphi c models , i f anything, are closer to the reality of animal behavior than mathematical ones. Needless
to say , models ar e not proofs ; they ar e suggestions. Models ca n help on e devis e
experiments and plan the collection o f data to test interpretations. We use humans
as a model only to improve our understandin g of the behavior of other organisms
and th e logi c behin d thei r behavior . Afte r all , mathematica l modelsmuc h i n
vogue among zoologists thes e daysar e als o just that: models, which have to b e
tested, an d which may or may not reflec t reality .
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PARTNERS I N COMMUNICATIO N
food plentiful , an d i f there ar e few mimics, then th e ris k of its mistakenly eating
the poisonous pre y may outweigh th e small benefit it gains by eating a mimic. But
the greate r th e numbe r o f mimics and th e scarce r the predator' s food , th e mor e
tempting th e cheater s become , an d th e greate r th e ris k t o the m tha t a predato r
will learn t o distinguish betwee n the m an d their poisonous model . A t that point,
the mimics' prominent colorin g become s a severe drawback.
SIGNALING TO PRE Y
Not al l communication betwee n pre y and predato r run s fro m th e forme r to th e
latter. The interaction betwee n th e tiger and the bull convinced us that predator s
may signa l their pre y as well. Th e tiger , onc e ther e i s no chanc e it ca n catc h th e
bull by surprise, moves in an arc around it. The bull endeavors constantl y to fac e
the tige r an d point it s horns a t it, to prevent th e tiger fro m pouncin g o n its back.
The tiger, indeed, i s looking fo r a n opening t o d o jus t that, while tryin g to avoi d
the bull's sharp horns. The tiger's black and white ears, which point forward, make
it eas y to tel l exactl y what th e tige r i s looking a t an d s o telegraph it s intentions .
Thus th e tige r force s th e bull t o react ; the tiger ca n then bette r asses s the agility
of th e bull , its abilit y to defen d itself , an d it s weaknesses. This informatio n help s
the tige r attac k whe n an d wher e i t i s sur e t o hav e a n advantag e ove r th e bull,
without running int o its horns .
The tiger is telling the truth. It makes real preparations
for attac k an d stop s i f and whe n i t i s clear tha t th e bul l
is read y t o repe l th e attack . Th e tige r want s t o fin d a
weakness i n th e bull' s defenses ; the mor e precisel y th e
predator display s its location an d its intended moves , the
more reliabl e an d informativ e the bull's reactio n is , and
the easie r i t i s for th e tige r t o identif y tha t weakness. If
the tige r di d no t displa y it s positio n an d movement s
clearly, it could not rely on its prey's responses and might
then underestimate the bull' s agility , strike, and find itself
impaled o n the bull's horns .
The interactio n betwee n tige r an d bul l i s simila r t o
that between two boxers in a ring. They do not as a rule go directly for a knockout
blow bu t firs t attemp t explorator y punches . A majo r blo w tha t misse s it s target
would thro w th e attacke r of f balance an d leav e hi m vulnerable . Boxer s usually
start with blow s tha t ar e strong enoug h t o forc e th e opponen t t o defen d himself
but d o not involve too great a risk. The exploratory punches test the ability of the
opponent t o react . A knockou t i s usuall y attempte d onl y afte r th e attacke r ha s
assessed his rival.
Some se e these explorator y punche s a s efforts t o mislea d th e opponent . Bu t
Prey-Predator Interactions 1
misleading i s a less effectiv e strateg y than on e tha t utilize s rea l advantages, since
its success depends o n the opponent's stupidity and on chance, rather than on the
attacker's rea l ability. Early in a bout, man y o f a boxer's move s ar e made t o determine th e opponent' s agilit y in defense . W e believ e thes e exercise s hel p th e
fighteror th e predatorno t b y misleadin g bu t rathe r b y offerin g precis e
information abou t th e attacker' s repertoire . Th e mor e reliabl e th e informatio n
provided b y the attacker , the more he finds out; eventually, he can attack what he
has learned are his opponent's most vulnerable points. The defender has no choice
but t o sho w the attacke r something of his defensive ability. Of course , a defender
certain of his strength and prowess may choose to ignore the attacker's maneuvers,
showing a cal m an d a lac k o f respons e which themselve s ma y persuade th e ag gressor of the defender' s abilit y to withstand a n attack.
Eshel16 also suggested tha t predators ma y communicate with their pre y in order t o identif y th e mos t vulnerabl e individuals . The predato r let s th e prey know
of it s presence ; a t tha t point , difference s i n th e behavio r o f th e potentia l pre y
help the predato r discer n which are the most vulnerable . Kruuk 17 describe s how
spotted hyena s choose prey among a herd o f gnu: one or several hyenas rush into
the herd, then stop and survey the fleeing prey. Only when they find an individual
in worse shape than the others d o theyand any other hyenas who may be watching fro m th e sidegiv e chase . Even afte r suc h selection , onl y 30 t o 4 0 percen t
of suc h chase s ar e successful . Th e prohibitiv e odd s agains t the hyenas ' catching
a physicall y fit gnu mak e crysta l clear their interes t i n communicatin g wit h thei r
prey.
The distanc e fro m whic h th e predato r "announces " itsel f mus t no t b e to o
great, though : otherwis e al l the pre y animal s will b e abl e t o escape . Eshe l suggested that th e color s o f leopards an d other spotted cat s reflect this strategic fact.
The spots on the leopard' s coat merge into a uniform gray-brown , camouflagin g
the leopard , a s long a s the anima l i s to o fa r awa y from it s pre y t o pursu e i t effectively. Bu t the sam e spots becom e distinc t a t closer range , making the leopar d
stand ou t an d announcin g th e terribl e menac e t o it s prey , whic h the n panic ,
showing the leopard whic h individua l it ought t o pursue. Lions, which ar e larger
and hun t i n groups , see m t o choos e individua l pre y les s selectively . Thei r col oration, which i s equally cryptic at all distances, enables the m to com e very close
and tak e prey by surprise.
12 P A R T N E R S I N C O M M U N
I CAT IO N
peated change s o f altitude , an d s o on . Thi s curiou s fligh t pat tern ha s commonl y bee n though t t o b e a communa l defens e
system: the errati c turning s o f the flock were believe d t o mak e
it mor e difficul t fo r th e rapto r t o targe t a particula r starlin g
without collidin g wit h another . Bu t Eshel 18 suggeste d a n addi tional explanation: that the maneuvers, which afte r al l are phys.j^ically strenuous , ma y be a strateg y by which th e starling s for
the weakes t o f their numbe r t o fal l behin d a s quickly as possible, to becom e eas y prey for th e raptor . Tha t serve s the interes t
of al l othe r member s o f th e flock , wh o thereb y avoi d a long ,
exhausting chase.
Prey-Predator Interactions
13
do not perish , o r d o not reproduc e t o the sam e degree. Bot h predato r an d prey
are probably unaware of the significance of their behaviors, just as they are unaware
of the functioning of their brains, their kidneys, or their muscles. There is no reason
to admir e these behavior s an y more than we admire the functionin g of other biological mechanismso r any less. All are marvels that deserv e ou r appreciation .
C H A P T E R
COMMUNICATION
BETWEEN RIVAL S
arely attack each othe r withou t firs t signalin g their intentions . Most
of th e time , the y d o no t attack a t all , an d th e conflic t betwee n the m i s
resolved b y a n exchang e o f threats . Thes e signal s com e i n man y forms :
singing, aerial displays, electric pulses (in the electri c eel), puffs o f noxious chemicals, posturing . Th e son g o f th e nightingal e advertise s th e bird' s readines s t o
defend it s territory and deter s its rivals. Red deer walk side by side and roar. Fish
swim in parallel to one another, extending their fins.
What about humans? There is a common notion, endorsed b y Konrad Lorenz,
that th e tendenc y to escalat e conflict s int o comba t an d th e readines s t o kil l opponents i s unique among humans. 1 But in fac t th e typica l study of animals done
at the tim e simply did no t las t long enoug h fo r researcher s t o determin e this. I n
most long-term studies observers have recorded conflicts that escalate into fights,
which have occasionally resulted i n woundings and eve n death. In our own longterm study of the babblers at Hatzevaover 20,000 person-hours of observation
there have been eyewitness accounts of some 20 fights that resulted in killings; we
have found indirect evidence that several more have occurred.
Among humans, too, most conflicts are resolved by threats rather than by actual
violence. Thi s i s true in particular on the persona l level, but als o on the interna 15
16 P A R T N E R
S I N COMMUNICATIO N
17
increased risk is acceptable to the honest signalerth e one who thinks the objec tive is worth a fight, and tha t it ca n win agains t that particular opponent. Such a
threatener ha s alread y decided t o fight if its opponent doe s not retreat , an d th e
increased likelihood that it will actually have to fight does not deter it. A bluffer
one who tries to gain by threats alone but i s not really willing to back up its threats
by fightingwoul d fin d th e increase d likelihood o f being attacke d to o risky . A
quick look a t known threa t signals illustrates this point .
THREATS BY APPROACHING
Threatening b y approachin g a riva l i s ver y commo n indeed . Approachin g i s a
reliable threat because by approaching it s rival, the signaler opens itself to attack.
If suc h signals were a pure convention, then an y movement would b e a s likely as
any othe r t o tak e on th e meanin g of threat. If the mos t clearl y visible movemen t
were the aim, then a movement sideways would have been better than a movement
forward or backward . But a movemen t sideway s is less risk y and thus , thoug h
clearer, is less reliable. Likewise, if signals were arbitrary conventions, a movement
backward would have been just as likely to become a threat as a movement forward.
We kno w o f n o case , however, i n whic h a movement awa y fro m one' s riva l has
become such a signal.
The stanc e o f th e defian t human male is well
known to us all: a straight back, the chest thrown
out, th e shoulder s back , chi n up . Thi s i s a very
inefficient an d risk y postur e i n whic h t o ente r
hand-to-hand combat . Th e uptilte d chi n i s ex posed t o blows ; th e erec t bod y make s it difficul t
for th e threatener to launch a surprise attack or to
change position a t all. It is the exac t opposite o f a
boxer's o r wrestler' s stanc e in th e ring : ready to
attack or avoid an attack, the boxer keeps his chin
down, clos e to his chest, and his body coiled lik e
a spring ; he balances on th e ball s of his feet , o n th e alert, ready to seiz e the first
opportunity. O f course , boxer s canno t resolv e th e matc h b y threats : both hav e
already committed themselves to fight.
The threatener , b y contrast , uses precisely this vulnerability to strengthe n his
threat. B y standing up straigh t he gives up th e benefi t of a good defensiv e stance
and th e option of a surprise attack. In the day s before razors, a man's thrown-out
chin presente d anothe r risk : it brought the threatener's beard nearer to his rival
and mad e i t easie r for th e latte r to gra b it . B y putting his chi n out , a threatene r
shows his confidence that his rival will not dar e or will not be able to grab him by
the beard or punch hi m on the chinand that he, the threatener, is still confident
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of winning the fight if the othe r does dare. A version of this signal is familiar fro m
a hundre d movie s an d cartoons : th e toug h gu y points to hi s outthrust chi n an d
taunts, "C'mon, big shot, lay one on me! "
THREATS BY STRETCHING-DECEIT OR
EXPOSURE TO DANGER?
Many animal s threaten b y stretchin g thei r bodies . I n suc h cases , th e threatener s
do no t sho w thei r weaponsteet h o r clawst o their opponent s but rathe r expose thei r whol e bodie s t o attack . Threatenin g dogs , a familia r example , stan d
side by side o n tiptoe , bodie s stretched an d hai r raised. 4 Suc h a posture i s commonly explaine d a s an attemp t b y the threatene r t o presen t itsel f a s bigger tha n
it reall y i s an d thu s t o dete r rivals. 3 Th e stretche d bod y doe s indee d provid e
precise informatio n abou t th e threatener' s size , bu t stretc h a s it may , no anima l
can becom e bigge r tha n i t reall y is , an d th e smalle r o f th e tw o wil l stil l see m
smaller tha n th e other .
Stretching is therefore not likel y to make a rival
misjudge one' s size . I s i t done , then , t o sho w off
one's actual size? Apparently not: eve n rival s wh o
know eac h othe r well , suc h a s longtime neighbor s
who ar e wel l awar e o f eac h other' s tru e size ,
threaten b y stretching their bodies. Th e only point
in signalin g is to affec t th e other' s behavior , an d a
fact that is known already is unlikely to change that
behavior. Keepin g it s bod y stretche d expose s th e
threatener to risk; why take a risk in order t o convey information that the rival has
already?
The point o f the stretche d bod y is not t o show size but t o conve y confidence.
Key t o an y predictio n abou t th e result s o f a figh t i s th e willingnes s o f a give n
individual to inves t i n that fightin other words, it s motivation. One wh o is not
sure the objec t of the fight is worth th e risk of injury will hesitate before exposing
its bod y t o danger . Motivatio n change s wit h circumstancesunlik e bod y size ,
which is easily determined an d doe s not chang e from da y to day. The appearance
of anothe r riva l o n th e scene , th e approac h o f a predator , th e soun d o f one' s
offspring callin g for helpall can instantly change one's willingness to take risks.
Thus, stretchin g one' s bod y i n th e presenc e o f a rival i s a reliable, moment-by moment indicator of one's current willingness to engage in the prospective conflict.
Such stretching displays often las t for a good while before coming to a resolution:
Glutton-Brock and his colleagues describ e red dee r walking in parallel along their
THREATS BY VOCALIZATIO N
Morton8 notice d tha t i n vertebrates, threatenin g vocalizations are usually low in
frequency, i n contrast to appeasement calls , which are more high-pitched. Morton
also observe d tha t large r individuals usuall y have lower voice s than smalle r one s
and suggeste d that a low-frequency cal l is intended t o reflec t th e threatener's size.
This raise s a number o f questions: Whe n rival s are looking a t each other, why
should they use hearing rather than sight to assess each other's size ? If a low voice
can frighte n rivals , ho w i s i t tha t animal s hav e no t simpl y evolve d longe r voca l
cords, so as to threaten better? And most of all, during conflict, why does the same
individual emi t high-pitche d sound s when frightene d rathe r tha n stickin g to th e
lowest-pitched sound s it can make?
The pitch of the voic e reliabl y discloses th e tensio n o f the signaler' s body. 9 A
tense bod y make s a more high-pitche d soun d tha n a relaxe d one . A frightened
individual i s tensed t o tak e flight or t o fight back. Onl y on e who is relaxed, no t
poised t o tak e instant action , ca n sound a low-pitched, threatenin g note . Suc h an
individual disclose s reliabl y that i t doe s no t fea r it s rival ; i t i s no t coile d lik e a
tightly wound sprin g an d thu s has exposed itsel f t o a first strike. Thisth e cos t
2O P A R T N E R
S I N COMMUNICATIO N
21
and tensio n versu s relaxatio n i s irrelevant. In suc h case s the voca l signa l conveys
other qualities . On e o f them w e have learned , a s we have s o many things, fro m
the babblers. " Th e long-distanc e threa t cal l o f babblers is a sequence o f several
loud syllable s clearl y separate d b y precise intervals. I t give s a good indicatio n of
the motivation o f the calle r and its willingness t o fight. When a group o f babblers
advances toward a border clas h with anothe r group, one can easily distinguish the
calls of the front-runner s from th e call s of those lagging behind. Th e one s in th e
front emi t rhythmi c and clearl y defined syllables; those i n the rear , who see m less
eager to fight, emit softer sounds , with less precise intervals. Once the rival groups
engage, th e call s o f those actuall y fightin g becom e metallic and highe r i n pitch ,
and the intervals between th e syllables are less precise. One can "hear" the tension
in their bodies .
Why d o th e babbler s use precisely space d syllable s onl y when the y ar e eager
to fight? In order t o emit rhythmic, regularly spaced, an d clearly defined syllables,
one ha s t o concentrat e o n th e ac t o f calling . An y distractionsuc h a s a glance
sidewaysdistorts bot h th e rhyth m an d th e precisio n o f sound ; a n individua l
cannot a t one an d th e sam e time collec t informatio n an d concentrat e o n performance. A cal l compose d o f precise , rhythmi c syllable s testifie s tha t th e calle r is
deliberately deprivin g itself of information, which mean s either tha t it is very sure
of itself or that i t is very motivated t o attack , or both. 12 A human being in control
of a situation, too , tend s t o issu e threat s i n a n ordered, rhythmi c cadence . Th e
even bea t increase s the effectivenes s of the threat , sinc e it show s confidenc e and
demonstrates th e threatener's abilit y to concentrate on the threat regardless of the
fact tha t h e or sh e may thus be deprive d o f crucial information.
OTHER THREATS
Staring a t a rival also impairs one's abilit y to collec t in formation; the risk is small for a dominant individual, who
is not likely t o be attacke d from behind in its own territory or group, but i t may be too high for one less in control of its surroundings. Hence , starin g is perceived a s a
threat. Th e individua l tha t stare s is dangerous eithe r be cause i t i s dominan t withi n it s grou p o r becaus e i t i s so
highly motivated t o attack that it does no t see k to gather
all the informatio n it can.
Contempt ca n als o be use d t o dete r rivals . A Holly wood sherif f enterin g a rustler's hideout with arms folded
and pistol s holstere d i s showing hi s confidence : if he were t o ente r gu n in hand,
it migh t increase the chance s o f an immediate victory, but b y displaying his confidence, he may get his man without the need for any gunplay. Likewis e one who
22
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turns his back o n a rival shows his contemptand his confidence ; a dog turning
aside t o urinat e i n th e middl e o f a confrontatio n show s i t i s confiden t tha t hi s
opponent wil l no t dar e attack himan d that i f attacked, he will stil l win, eve n
when caugh t with one leg in the air.
Still another wa y to issu e a threat i s to sho w the degre e of harm one is willing
to suffe r i n orde r t o win . When ant s us e formi c acid an d bee s us e chemical s in
their fighting , the y creat e a n environmen t hostil e t o bot h signale r an d rival . I t
makes sense that one able and willing to endure the noxious chemicals displays in
a reliable way its ability and commitmen t to the fight.
24 PARTNER
S I N COMMUNICATIO N
C H A P T E R3
MATE SELECTION
26 PARTNER
S I N COMMUNICATIO N
flashes of light. Moths and many mammals emit scents. Even one-called organisms
like yeast and alga e emit pheromones t o attrac t mates.
Sometimes bodil y growth s ar e mean s o f sexua l display: newts gro w a finlike
nuptial cres t alon g thei r backs; the whit e pelican grow s a bump o f flesh between
its eyes . The male s of many bird specie s suc h as shrikes, terns, an d gulls , as well
as some insects, court their mates with nuptial gift s o f food, leaves, or twigs. Male
bowerbirds buil d comple x bower s an d decorat e the m wit h shell s an d flowers,
bones, insec t skeletons , an d colorfu l fruits t o attrac t females ; som e male fish and
crabs buil d san d castle s o n rock s expose d t o th e waves , castle s that hav e to b e
continually rebuilt.
The extravagan t dimensions o f sex ual displays make them see m like crazy
fashio
n shows . Bu t hav e the y ru n be yon
d reasonabl e evolutionar y control ,
a
s s
i commonly assumed? Or do the dimensions o f th e display s an d th e spe cific form s they take serve a purpose?
Mate Selection 1
28 PARTNER
S I N COMMUNICATIO N
a mal e who ca n barel y fee d himself . It als o prevents male s from courtin g many
females simultaneously .
White pelicans , bot h mal e an d female , gro w
fleshy bumps between their eyes when they are
ready to breed. The bump interferes with the pelican's ability to see the area around the tip of its bill.
In orde r t o catc h prey, a pelican with a bump ha s
to remember where it last saw its prey and project
the prey's likely movements. An inexperienced or
inept pelican would not be able to do so. A pelican
that can fish and maintain itself in spite of the handicap of its bump is reliably demonstrating its expertise in fishing. Later, when th e
pelicans hav e t o fee d thei r brood o f fou r o r fiv e demandin g young , the bum p
shrinks an d they are able again to hunt mor e efficiently .
Singing can also demonstrate the ability to provide. The time invested in singing
cannot be use d fo r foraging. A courting male who handicaps himsel f b y singin g
continuously provide s evidenc e tha t h e needs les s tim e to forage , eithe r becaus e
he is very efficient o r because his territory is very rich. Wilhelm and his colleagues3
studied the effec t o f supplementary feedin g o n the singin g o f yellow-bellied sunbirds. They found that males who were not given insects did not sing, while thos e
who receive d insect s an d suga r wate r san g ofte n an d a t length . Tim e spen t i n
sentinel activity, or in dancing displays, can also indicate expertise in finding food,
especially when the "waste " of time comes early in the mornin g after a long, cold
night without food.
Superterritories
O'Donald6 ha s suggeste d tha t th e siz e o f a n animal' s territor y ca n serv e a s a n
advertisement. Male s an d female s o f man y species protec t a territory an d chas e
others away from it. Often the territory is far larger tha n is needed to provide food
or shelte r fo r a pair o f mates and thei r offspring. Som e suggest that these bigge r
territories preven t overexploitatio n o f food resources , and thu s a richer resourc e
remains t o sustai n th e populatio n a s a whole i n th e future. 7 Bu t thi s argumen t
depends o n th e mechanis m o f group selection , which, a s we have seen , i s questionable. Whe n som e males protect territorie s tha t ar e larger than the y need, th e
population a s a whole might gain from th e preservatio n o f future foo d resources;
but th e males who hold smaller territories would gai n the most, since they would
enjoy th e resource s preserve d b y earlier resident s withou t squanderin g thei r own
efforts protectin g large r territorie s tha n the y need; the y would therefor e be abl e
to devot e mor e o f their energ y t o reproduction . Thus, ove r th e generations , th e
tendency t o hol d a larger territor y than one needs woul d disappear . Why , then,
Mate Selection 2
Courtship Vocalization
Many animals vocalize during courtship . Lions , tigers, and dee r roar ; cicadas and
crickets chirp ; bird s sing . Courtshi p call s ca n b e dangerous : Ryan an d hi s colleagues8 showe d tha t frog-eatin g bats locat e frog s b y th e amphibians ' courtshi p
calls. Onl y a mal e frog tha t ca n successfull y avoi d bats despit e disclosin g its location t o the m ca n affor d t o croa k much . Courtshi p call s ca n als o be ver y demanding: Glutton-Brock and Albon 9 found that red deer are often exhauste d afte r
a roaring contest with rivals. Only a strong, well-muscled individua l ca n roar loudly
for a long time.
The detail s o f a call , it s tempo , an d th e numbe r o f syllable s in a phrase ca n
demonstrate th e caller' s quality . The son g o f th e grea t tit i s a series o f precisely
spaced syllables . Lambrechts and Dhondt 10 found a positive correlation betwee n
3O P A R T N E R
S I N COMMUNICATIO N
Colors
The adul t males o f many species o f birds ar e far more colorfu l tha n female s an d
young males: examples include peacocks, ducks , birds o f paradise, an d sunbirds .
Colorful plumag e attracts rivals and predator s an d thu s serves as a reliable signal
of quality : only males of high qualit y can risk advertising their location. Conspic uous coloratio n als o emphasixe s the exac t shape , posture , an d movement s o f its
bearer. A high-quality individua l "wears " brigh t colorin g well ; o n a low-quality
one the sam e coloring accentuate s imperfections. 12
Scents (Pheromones)
Scents also serve to attract mates. Studies have found that some female insects can
identify a dominant mal e by its scent alone. 13 Many male mammals, too, use scent
to attrac t females and dete r rivals . We kno w a great dea l abou t th e chemistr y of
pheromoneschemicals that are produced by one individual in order to influence
the action s o f others ; bu t ver y few scientist s hav e trie d t o explai n th e adaptiv e
significance o f specific chemicals. It woul d b e fascinatin g t o discove r wha t infor mation the pheromone s o f each specie s provide abou t thei r producers .
The mai n componen t o f the pheromon e secrete d b y male arcteid an d danai d
butterflies i s a derivative of a n alkaloida stron g poiso n produce d by plants fo r
their ow n protection. 14 Arctei d larva e ca n metaboliz e th e poiso n an d thu s tak e
advantage of a food sourc e that is not availabl e to most other animals ; the poiso n
that the y take into thei r syste m then help s protec t the m fro m predators . A male
arcteid butterfl y secretin g thi s pheromon e testifie s tha t a s a larva he wa s able t o
feed o n the poisonous plants ; the concentratio n of poison i n the pheromone demonstrates th e male' s relativ e physiological abilit y to dea l with the poison . Danai d
butterflies secrete a similar pheromone, derive d from plants that they eat as adults.
Eisner an d Meinwal d furthe r propose d tha t th e pheromon e coul d functio n a s a
chemical yardstick by which females gauge the poison load their suitors carry . The
alkaloid i n the pheromon e ma y also sho w tha t th e mal e will probably b e abl e to
Mate Selection 3
32 P A R T N E R
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and builder befor e deciding whether to copulate wit h the hopeful candidate. The
female copulates onl y once before egg-laying. She may well visit a bower, examin e
it, watch the male perform hi s dances, even take part in the dancing and court the
male befor e decidin g t o pas s him up . I t seem s tha t th e decoratio n o f the bowe r
plays a large part in the female' s choice o f a father for he r offspring .
The numbe r o f decoration s i s importan t t o female s too . The y prefe r male s
whose bowers are richly decorated. Male s steal decorations from neighboring bow ers. Borgi a trie d addin g individuall y marked rar e an d sought-afte r ornament s t o
one se t o f bowers , the n t o another ; h e foun d tha t n o matte r whic h bower s h e
added the ornaments to, they always wound up in the bowers of the most successful
males.20 To be attractive to females, a male bowerbird has to spend considerable
time an d talen t buildin g hi s bower , collectin g decorations , placin g them , an d
guarding them agains t hi s neighbors, not to mention performing o n the stag e he
has built. He thus proves that he is stronger and more energetic than his neighbors,
that h e ca n fee d himsel f adequatel y an d i s stil l abl e t o buil d an d decorat e hi s
elaborate bower , guar d it agains t competitors, an d raid their bowers. 21
When w e visited Borgi a in Australia , we sa w some bower s o f the grea t bow erbird. Th e platfor m a t th e entranc e t o th e avenu e include d fla t stone s fro m a
riverbed, bleached bone s (mostl y vertebrae), broken glassmos t of it greenand
colorful bit s o f foi l an d cardboard . Borgia observe d tha t th e arrangemen t o f th e
decorations wa s not random . Th e gree n bit s o f glass were consistentl y placed by
the norther n entry , whic h i n th e souther n hemispher e face s th e sun . Th e glas s
glistens i n th e sunlight , an d th e mal e display s his viole t plume s agains t a shiny
color-coordinated backdrop .
Combinations of Signals
In mos t cases , severa l signal s of differen t kind s ar e use d i n courtship . I n birds ,
special feathers , brigh t colors , singin g an d calling , dancing , and gift-givingth e
last thre e of which deman d tim e and energyal l pla y their part . Eac h modalit y
brings out a particular qualit y of the male; the female can then use several criteria
to asses s the male . Let's tak e the displa y of the peacock a s an example. Th e mal e holds hi s tail uprigh t
and spread outwhich demands considerable effort .
From tim e to tim e he shake s his tail vigorously; this
requires ye t more effor t an d produce s a remarkabl e
rattle. Th e "eye " pattern s o n th e peacock' s tail , the
glisten of his feathers, the crow n o n his head, all add
up to a symphony of shape, color, pattern, movement
and sound a performanc e tha t i s announced wit h
periodic roars .
Each aspec t of the displa y seems to convey specific, reliable information about a
particular featur e o f th e male . Th e lon g tai l feather s ar e grow n ove r a period o f
Mate Selection 3
several months, during a time of the year when food is scarce. Unhealthy birds arrest
the process , s o a male who display s a set of perfect tai l feathers advertises that h e
has been i n good health an d has managed to find food even during molt season .
The long , heavy, brightly colored tai l als o attest s to th e owner' s strengt h an d
skill, for he has succeeded in avoiding predator s despite such a burden. By holding
his tail upright an d shaking it, the peacock proves his stamina, and his roars show
he is not afrai d t o disclos e hi s location t o rival s and predators. The perfection of
the tail' s pattern testifie s tha t th e peacock' s developmen t whil e the tail grew was
perfectly coordinated , a s we shall see in chapter 8 . Each of these criteria seems to
be minutel y scrutinized b y females: Petrie an d he r colleague s foun d tha t takin g
out eve n five of the hundred an d fifty or so feathers in a peacock's tail reduces his
ability to attract females to his dancing arena. 22
Long Tails
Moller23 investigated the long outer tai l feathers of barn swallows, small songbirds
that catc h thei r foo d i n flight . Bar n swallow s hav e long , forke d tails ; th e oute r
feathers ar e longer i n adul t male s than i n females or in young males. When Molle r adde d
extra pieces of tail feather to the tails of some
males an d shortene d th e tai l feather s o f others, he discovered that thos e with th e longer
tails, whether natura l or artificially enhanced ,
found mate s more easil y than thos e with th e
shorter or shortene d tails , and tha t the y got
to copulat e wit h additiona l female s a s wel l
(extrapair copulation) . Bu t th e inadverten t
cheatersthe male s wit h artificiall y length ened tailspai d a heavy price. The added length apparently impaired thei r ability
to fly. They could not hunt large insects, and their physical condition deteriorated :
they did not molt well afte r th e breeding season , and none of them returne d from
their winter migratio n the next spring , while many of the other male s did retur n
to breed i n the same area.
Smith and Montgomerie 24 repeated Moller's experiments and found that males
with eithe r naturall y long o r artificiall y lengthene d tail s found mates earlie r an d
started breeding earlie r tha n othe r swallows . Bu t when the y teste d fo r paternit y
among the nestling s by DNA fingerprinting, they found that only half of the nestlings i n the nest s o f the inadverten t "cheaters"th e males with enhanced tailswere i n fact th e offsprin g o f those males , compared wit h 9 5 percent i n the nest s
of male s whose tail s were eithe r naturall y long o r artificiall y shortened. 25 Smit h
and Montgomerie suggested tha t the glued-on tails were too much of a burden for
males who were not fit to carry them, and that suc h males could not prevent their
females fro m consortin g with other males.
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The experiments o f Moller and of Smith and Montgomerie with barn swallows,
and o f Evans an d Thomas 26 wit h th e scarlet-tufte d malachite sunbird , sho w th e
price paid b y a bird wh o carrie s a longer tai l tha n h e ca n handle. Thu s it woul d
seem tha t longe r tails , like the bar n swallow's , th e peacock's , an d thos e of many
other birds, are reliable indicators o f the agilit y of strong, experience d bird s and
are attractive to female s for precisely that reason .
Mate Selection 3
paradise, males court an d displa y in leks; among ruffs an d sag e grouse, hundred s
of birds may congregate in one lek.
Lekking males do not have equal success in reproduction. Mos t males ultimately
do not copulate a t all; two or three maleswho are usually in the center of the lek
may d o ove r 9 0 percent o f the copulating . Why , then , d o th e othe r male s com e
together where the y hav e little to gain ? Probably because elsewhere thei r chance s
are smaller still. Petrie an d her colleagues note that on days when many females visit
the top male, other males may attract some females too.28 Hoglund and his colleague s
found tha t the more males in a lek of ruffs, th e more females there are in proportion
to males.29 Females, afte r all, find it easier to choose a father for their offspring when
they ca n compar e males side by side . Mor e tha n on e femal e ca n affor d t o choos e
the same male; they do not mind sharing him with others because they will not have
his help in raising their young anyway. Under such circumstances, it is in the interest
of female s to b e abl e t o compar e a s many males a s possible, as easily a s possible.
Gibson an d Hoglund foun d that young female grouse tend to prefer males selected
by older, experience d females : they watc h th e experience d ones , the n choos e the
same males. 30 If fo r thes e reasons females ignore small congregations of males an d
insist on the greater choice afforded b y larger ones , males are forced to compromis e
with other males and congregate .
Manakins ar e smal l birds o f th e America n tropic s
that displa y in leks.31 Among them there are males who
dance in a miniterritory within the lek in groups of two
to five. Only th e to p mal e of each group, wh o i s olde r
than the others, copulates with the females who visit the
courting arena . Th e other s cooperat e wit h hi m i n th e
dance without immediate reward; but som e of them can
benefit i n the long run. After hi s death, it seems that his
top helper , wh o is usually at least six years old, inherits
the top male's miniterritory. 32
Female manakins seem to prefer the group performers. No wonder : th e to p mal e in a group aren a demonstrates both his dancing ability and the deference that other males pay him, which
makes hi m al l the mor e attractiv e to females . The othe r member s o f the grou p
gain a s well: the y ca n both practic e thei r dancin g an d increas e their chance s to
inherit a good miniterritory.
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Mate Selection 3
38 P A R T N E R
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and reproduce d whil e other s di d not . Thi s theory , thoug h genera l an d all encompassing, di d not explain th e waste involved in the showing of f that precedes
sexual reproduction . Darwi n coul d no t se e ho w a n investmen t i n showin g of f
increases a n individual's efficiency . H e suggested , then , tha t ther e ar e two kind s
of selection : natura l selection, whic h make s a n animal best suite d t o it s environment, and sexual selection, which assists an animal in competing within its gender
for th e chanc e to reproduce .
Darwin38 thu s define d sexua l selectio n a s competition wit h member s o f th e
same sex. With thi s definitio n Darwin lumpe d togethe r straightforward , efficient
fighting between riva l suitors with features that enable an individual to deter rivals
of the sam e species and gender by means of threats, and with features that attract
potential mates. Darwin di d no t se e a problem i n the evolutio n o f bizarre signals
that functio n i n sexual advertisementhe simply turned his observations into an
explanation. Th e simpl e fac t tha t bizarr e signal s attrac t mate s an d dete r rival s
justified fo r him the investment animals make in these signals. He di d not as k why
waste attracts mates and deter s rivals . Rather, he treated these effects a s a given.39
In th e earl y twentieth century , Fisher recognize d th e proble m presente d b y
animals' preference for wasteful signals. He stated , rightly , that female preference
is an adaptation like an y other produce d b y natural selection; h e then aske d why
females prefe r wasteful males.40 The mode l Fisher propose d t o answer this question use d to be the only one available, and many still believe i n it. The model can
be found in almost any book o n evolution. 41
Fisher believe d tha t th e mal e who show s of f is no bette r tha n th e mal e who
does not sho w off. According t o that premise, th e showing off itself is a drawback ,
and thus the show-of f males are less well adapted than their fellows. 42 According
to Fisher , th e onl y advantage the ostentatiou s male s have is the fac t tha t females
consider the m attractive . Since such males pass on the show-off character to thei r
offspring, thos e offsprin g wil l show of f and wil l be attractiv e to female s too. According to thi s script, male s gain by investing in showing off because by showing
off they attract more females. Females lose by having offspring who waste resources
on showin g off , but the y have n o other choice : onl y wastefu l offsprin g wil l b e
attractive to other females, wh o in turn will have inherited from thei r mothers the
tendency to be attracte d to wastefulness.
Fisher's mode l ca n be see n a s a catch-22, in which each individual male in th e
population waste s resource s o n showin g of f solel y becaus e thi s i s the accepte d
method o f courtship i n his species. Severa l mathematical models support th e ide a
that onc e som e of the populatio n conside r a particular random featur e to b e attractive, the n a "runaway " proces s ma y develop b y which th e featur e spread s
quickly throughou t th e population . I n suc h a population , a femal e wh o wen t
against the trend and selected a male who is more efficient an d shows off less might
have mor e efficien t mal e offspringbu t thes e offsprin g woul d fin d themselve s
without mates , since other female s would no t choos e them.
Fisher assume d that th e proces s start s when som e females, who selec t a male
Mate Selection 3
4O P A R T N E R
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P A R T I
METHODS OF
COMMUNICATION
C H A P T E RR4
THE FALLAC Y O F
SPECIES-SPECIFIC SIGNAL S
44 METHOD
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46 METHOD
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than individual s wh o di d no t carr y the sam e markings, unti l with tim e th e trai t
spread throughou t th e population. Th e early bearers of the markings had to have
some advantag e over individual s wh o di d no t bea r them . Tha t advantag e could
not b e tha t i t wa s easier t o identif y the m a s members o f the species , fo r a t that
point mos t members of the specie s did no t carry the markings.
makes it easier for group members to asses s the difference s amon g them. If each
person withi n th e grou p wor e wildl y differen t clothin g i t woul d b e difficul t t o
compare them with on e anothe r i n a meaningful way.
How exactl y can uniform decoratio n sho w th e
difference betwee n individuals ? Let's star t wit h a
simple example : let' s sa y we are going t o th e marketplace to find a handmade round plate. The plates
are not identical . Some were made by skilled crafts men and are perfectly round; others were less skillfully mad e and ar e slightly elliptical, or their edges
are a bit malformed . A small circle in the middle of
a plate would mak e it easier for us to tell th e most
perfectly round plates from th e less perfect ones . A line around the edge of a plate
would mak e it eas y to spo t imperfec t edges. If we wish to selec t perfectl y roun d
plates with neat , perfect edges , it would mak e sense for us to selec t fro m amon g
plates decorated wit h a circle in the middle and a line around the edge, even if we
have t o pa y a somewha t highe r pric e fo r them . Sinc e othe r shopper s ar e als o
looking for well-crafted round plates , it would mak e sense in turn for the skille d
artisan to paint a circle in the middl e o f each plate and a line around its edge.
This decoration wil l clearly benefit the makers of perfect plates, but why should
the maker s of less than perfect plates decorate them with a pattern that will bring
out thei r imperfections ? They should d o s o because they are competing with yet
other craftspeople, whose plates are even worse. Buyers who cannot find or cannot
afford th e best plates would thu s be reliably drawn to the better ones amon g the
ranks o f the imperfect . Eve n th e maker s of the absolut e wors t o f the plate s ha d
better invest in such patterns, since buyers will reject ou t of hand plates that don't
bear the pattern, and since there might appear an incompetent artisan making even
worse plates than theirs. The proces s is driven by the preferenc e of the buyers.
This issu e of choic e i s crucial. An essentia l condition fo r th e developmen t o f
any signal is that the receiver of the signal must have at least one other alternative
otherwise ther e i s n o chanc e o f affectin g th e receiver' s action s an d n o poin t i n
signaling to it . A gazelle can tel l a wolf reliabl y that it is an excellent runne r an d
that th e wol f ha s littl e chanc e o f catchin g it , bu t i f th e wol f doesn' t hav e th e
alternative o f findin g othe r prey , i t ha s t o tr y t o catc h tha t gazelle , even thoug h
the gazelle has just proven tha t the chas e will be a hard one.
If, a s we believe, animals ' markings evolved in order to bring out smal l differ ences betwee n competin g individuals within a species, then th e marking s cannot
be arbitrary. Not every decorative pattern would enable us to judge a plate's roundness equally well; many patterns would actuall y disguise imperfections and make
it more difficult fo r us to find the better-made plates. Likewise, any markings could
serve to identif y species , gender, or age . But i f species-specific markings show off
certain importan t trait s i n member s o f th e grou p wh o compet e t o prov e thei r
quality, th e markings that evolve have to be thos e that best brin g ou t difference s
48 METHOD
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regarding these traits . And indeed, onc e one starts looking a t animals with this in
mind, examples abound .
rumps. Many of the waterbucks were infested with ticks and were thin and weak.
Their white rumps made it easy to tell from behin d whic h antelopes were in good
shape an d which were thinner than the y should be . O n thi n antelopes , th e white
patch had the shape of a pointed ellips e because of the atrophied hin d leg muscles;
on healthy animals, the patch looke d nic e and round. Th e hind leg muscles are of
immense importance t o th e antelopethe y ar e its "engine, " its driving force. A
predator looking for eas y prey, a rival evaluating his chances in a contest, a female
looking fo r th e bes t fathe r for he r offspring , al l can benefi t from evaluating th e
muscles of the rump .
The wing s of many butterflies are outlined with
a narrow fram e o f color . I f the win g were uniform
in color , i t would b e difficul t t o spo t smal l defects
in the edge. The colored outline , on the other hand,
is visibl y broke n b y imperfection s i n th e wing' s
shape. Suc h breaks can result fro m developmenta l
defects, encounter s wit h predator s wh o tak e bite s ou t o f th e wing , o r collision s
with har d objects . They are more likely to occur i n older individuals . The outlin e
can enable females to spot broken edges and so avoid mating with males who have
birth defects , ar e clumsy, or have reached the ag e where they have spent most of
their sperm. Similar frames an d colore d edge s o n feathers enable birds to tell th e
condition o f those feather s at a glance.
Beaks, nails , hooves , fins , spines , tails , an d horn s ar e ofte n a differen t colo r
than th e body. The differenc e brings ou t th e shape , size , an d movement o f these
parts, just as among humans nail polish show s off the exact shape and movements
of nails and fingers .
5O M E T H O D
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SYMMETRY
The correlatio n o f symmetry to quality , both in animals and i n humans, has bee n
studied recentl y by several researchers; the term used in current literature is "fluctuating asymmetry. " Moller 17 foun d tha t th e mal e swallow s preferre d by females
had bot h longer an d mor e symmetrica l tails (tha t is, the lef t an d righ t part s were
evenly matched) than males who took longer to find mates. Research confirms that
humans conside r symmetrica l face s t o b e mor e beautifu l tha n somewha t asym metrical faces. 18 Thornhill 19 foun d tha t mal e scorpio n flie s wh o wo n fight s wit h
rivals, and who brought mor e presents to their mates, had more symmetrical wings
than the male s they defeated. It i s not clea r whether femal e scorpion flies actually
chose male s fo r thei r symmetry ; even whe n th e female s selecte d male s b y smel l
alone, without seein g them , the one s the y chose were more symmetrica l than th e
ones they passed up. What, then, is the connection between symmetry and quality?
Stress or geneti c flaws often caus e asymmetrical development o f body parts. 20
52 METHOD
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If the proble m wer e simpl y lack of nutrients or of energy, one would expec t that
deficiency t o affec t bot h side s o f the bod y evenl y and cause , say, a shorter symmetrical tail rather than a longer, asymmetrical one. W e believe tha t symmetrical
growth requires reliable communication within the body.21 For synchronized, symmetrical growth, the center that regulate s growth must send the same messages to
both side s of the body, get feedback on the results, and pace further developmen t
according to the data received .
As we shall see in chapte r 9 , signaling between cell s in the multicellula r bod y
requires reliability no less than communication between organism s does. It seems
that only a cell in good shap e can afford t o manufacture a quality signal. In other
words, reliabl e communicatio n withi n th e bod y demand s a n investmen t o n th e
part of the organism, and it may be that under conditions of stress the body cannot
spend enoug h o n suc h communicatio n to ensur e symmetry . Thus a symmetrical
shape indicates bette r overall healt h durin g development tha n a less symmetrical
shape.
An awareness and understanding of "esthetic" features such as symmetry, good
color, an d patterns that suit what they decorate thus bring real and concrete benefits t o thos e wh o posses s them . Indeed , in the las t chapte r o f this book we will
suggest tha t thi s connectio n betwee n "beauty " an d qualit y i s th e basi s fo r th e
evolution of the estheti c sense in humans.
The righ t decoratio n ca n revea l th e degre e o f symmetry. 22 A lin e dow n th e
middle of the body, or down the middle of a body structure, is an obvious example.
A circle in the middle of an area that ideally is symmetrical is another. In fact , any
symmetrical decoratio n o n bod y part s helps observer s asses s symmetry of shap e
and structure; and since the decoration cannot be more symmetrical than the body
parts themselves, the informatio n conveyed is reliable.
"EYE" PATTERN S
The peacock' s lon g tai l feather s take severa l months to
grow. The score s of tail feathers are arranged so that eyes
form arches ; the arche s ar e ver y orderly, wit h eac h eye
exactly halfwa y betwee n tw o eye s i n th e arc h abov e it .
Missing eye s are very conspicuousthere is no nee d t o
count, an d a peacock canno t hid e th e los s o r imperfec t
development o f eve n on e tai l feather . An d a s Petri e
found,23 th e respons e of peahens is measurably different i f even only five eyes are
missing in a peacock's tail , out o f a hundred fifty or more .
For a round ey e pattern to emerge on a lengthening feather , the entire growth
and developmen t o f that feather have to be in perfect synchronization. Any irregularity in development would ruin the perfection o f the circle. A circular pattern
and eve n more, a circle within a circleis thus ideal fo r displayin g regularity in
the proces s of growth. I f the peacock's tail were decorated with lines, it would b e
difficult t o b e sur e of deviations : a line o f on e lengt h i s not mor e perfec t tha n a
longer o r shorter line. But an imperfectly developed circl e exposes any distortion,
in an y direction.
This valu e of eyelike patterns can explain their widespread occurrence, a s on the wings of butterflies, mantids,
and other insects . Th e standar d explanationtha t th e
eyes frighten off predators, wh o mistake them for the eyes
of larg e animalsi s a n insul t t o th e predators ' percep tion; nor doe s it explain patterns composed o f many eyes,
or o f serie s o f four o r five concentric circles . W e doub t
that an y predator s ar e frightene d of f b y th e eye s o n a
peacock's tail. 24
54 METHOD
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will therefor e als o b e different . Individual s wit h decorativ e marking s tha t bes t
emphasize these new characteristics will have an advantage ove r individual s wit h
the old decorative markings, and the new markings will spread in the population .
First come s the evolutio n o f new adaptations ; next, individuals start focusing on
these adaptations; and finally, because of that attention, new decoration emerges
the ne w species-specific markings.
But the story is not alway s this simple. Sometimes members of the same species
have differen t markings . One suc h polymorphic species is the ruf f mentione d i n
the previous chapter . Some male ruffs hav e dark ruffs, other s have light ruffs. Th e
courtship behavior o f each typ e i s also different . Th e dark-ruffe d males ten d t o
hold a territory within the lek and dance in it, while the light-ruffed male s tend to
fly fro m on e territory to another, dancing with several of the dark-ruffe d male s in
turn. A s we discus s i n detai l i n chapte r 8 , blac k an d othe r dar k color s bette r
emphasize siz e and shape , while whit e i s better fo r showin g of f movement. Th e
darker colo r o f the territory-holder s better advertise s their stance , while the fac t
that th e light-colore d ruff s ar e s o ofte n i n motio n explain s wh y the y advertis e
themselves with lighter colors. We don't think that the difference i n colors evolved
so tha t wha t w e no w cal l th e dar k an d th e ligh t form s coul d b e distinguished ;
rather, we believe it evolved to enable each light-colored ruff to try to show himself
as the bes t amon g the light-colore d ruffs , an d t o allo w each dark-colore d ruf f t o
compete as successfully a s possible against othe r dark-colored ruffs .
The relationship between decoratio n an d its message
explains wh y it s o ofte n happen s tha t unrelate d specie s
who occupy a similar ecological niche look alike. The decoration of the deser t agamida e of the Middle East is very
similar to that of desert iguanas in the Americas, as is the
decoration o f rattlesnakes in Americ a an d tha t o f vipers
in the Ol d World . Lack remarked that bird s that liv e in
similar condition s ten d t o hav e simila r decoration. 26 I n
the Argentinean plains, we encountered what we thought
was a creste d larkonl y t o lear n tha t i t wa s i n fac t a
larklike brushrunner (Coryphistem alaudina). Species that
live i n simila r environments tend t o evolv e similar traits
to best dea l with these environments; they then advertis e
these traits with the markings tha t best show them off
which tend t o be simila r patterns and colors.
55
56 METHOD
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57
In sum , we believe tha t thos e markings that bes t dis play difference s i n qualit y o r motivatio n amon g similar
individuals evolv e t o become commo n t o the entir e species, o r t o a n ag e and gende r grou p withi n th e species ,
for precisel y tha t reason . Sinc e differen t specie s hav e
adapted differently , th e decoratio n appropriat e t o thos e
species would likewis e be different. Tha t others use these
differences t o identif y th e grou p t o whic h a n individua l
belongs i s a side effect o f the competitio n amon g individuals within th e group .
58 M E T H O D
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information. For example, one can judge the direction o f another's gaze by watching
its eyesye t ey e movement i s not primaril y a signal. But ey e rings and smal l tuft s
of hai r or feather s whose onl y function is to sho w a n observe r th e directio n o f an
individual's gaze more clearly, or from a greater distance, are signals.
The abilit y to observ e an d understan d signal s is an adaptatio n lik e any other
that evolves through utilitarian selection. An individual who pays attention t o unreliable signals will be less successfulwill have fewer descendantsthan one who
insists o n payin g attentio n t o reliabl e signal s only . A s w e hav e seen , reliabilit y
demands investmen t b y its very naturethe signaler's investment i n the signa l is
the guarante e of its reliability.
It is not always easy to judge whether a specific trait is purely a signal or whether
it has some other function, but i t is still important to make the distinction. What ,
then, i s th e fundamenta l differenc e between signal s an d othe r traits ? I t i s th e
relationship between th e signa l and it s cost. Ever y trait, whether a signal or not ,
demands an investment of some sort, and ever y trait is constrained by other traits
whose requirement s conflic t wit h it . I n thi s signal s ar e simila r to al l other traits .
Changes in the environmen t ma y change the constraint s on the evolution of traits
and lesse n o r increas e the cos t involved . For example , th e siz e of a n anima l may
be limited by its need to stay small and quick to avoid predators, but if its predators
are remove d i t ca n affor d t o increas e in siz e and thu s increas e it s ability to stor e
energy, withstan d cold , o r defea t rival s of it s ow n species . Th e specie s the n be comes larger because th e cos t of being big has gone down significantly .
If, o n th e othe r hand , th e cos t o f a signal is reduced t o th e exten t tha t every
individual can use it equall y well, the n th e signa l can no longer revea l difference s
in the qualit y or motivation of individuals. In suc h a case, the signa l loses its value.
Because the signal's cost has gone down significantly , the signal is no longer usefu l
and wil l disappear. 36 Th e evolutio n o f signalssigna l selectioni s thu s funda mentally different fro m th e evolutio n o f all other adaptations .
In trait s othe r tha n signals , the cos t of the trai t i s an unavoidabl e sid e effect .
In signals , cost is of the ver y essence; it is necessary to the existenc e of the signal.
If ther e i s no cost , nothin g prevent s cheater s from usin g a signal to thei r benefit
and t o the detrimen t o f the receivers , and that signal will lose its value as a signal.
This ha s happene d no t infrequentl y in huma n history . When mone y is easier to
get, i t loses value through inflation. Ornaments that were prized as tokens of wealth
when rar e became worthless when easy to obtain .
When lac e was made by hand by expert workers, the
amount of skilled labor needed to produce it made it very
expensive; lace costand was worthits weight in gold
to th e ric h an d powerful , wh o wor e i t t o displa y thei r
wealth. The developmen t o f machines that could cheaply
manufacture lac e indistinguishabl e fro m th e handmad e
product37 put a n end t o the use of lace as an indicator of
wealth; today , in fact , lac e i s not muc h use d a t all. 38 By
6O M E T H O D
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contrast, commodities lik e bread o r iron that ar e used to meet direct needs rather
than to sen d signal s do not los e their usefulnes s i f their pric e goes down ; rather,
they are used all the more.39 Although human cultural and economic developmen t
are differen t fro m biologica l evolutionar y systems, the tw o have a very important
common element: both emerg e from th e need competitors have to cooperate an d
communicate.
The significanc e of cos t i s unique t o ou r theor y of signa l selection. N o othe r
theory of signal evolutionand certainl y no theor y that assumes the existenc e of
agreed-upon, conventional signalswoul d predict that if its cost becomes low, a
signal wil l los e value. It shoul d b e possibl e t o tes t thi s hypothesis : eve n thoug h
experiments with evolutionar y processe s require many individual subjects an d a
long period o f time, they are feasible with unicellular organisms or organisms that
multiply rapidly.
Meanwhile, we can test our theory against observations of animals in the field.
As thi s boo k wa s goin g to press , we learne d o f som e finding s tha t suppor t ou r
view of the impact of inflation o n th e effectivenes s o f a signal. In Australia , male
satin bowerbirds especiall y favor blu e objects; in their usua l habitat suc h objects
consist o f blue feathers , whic h ar e rare , an d blu e flowers that need constan t re placement. Borgia 40 found on averag e five blue feather s pe r bower . Nea r human
habitats or picnic grounds, however, blue artifactsmostly blue plasticare fairly
common, and sati n bowerbirds ca n collect as many as a hundred pe r bower .
In mos t areas , male sati n bowerbird s compet e bot h by stealin g blue object s
from on e anothe r an d b y destroyin g each other' s bowers . Hunte r an d Dwyer 41
recently found , however, tha t wher e blu e objects ar e abundant, th e males direc t
less effort int o stealin g such objects from on e another, an d more into destructio n
of their competitors ' bowers, tha n the y d o i n areas wher e such objects ar e rare .
Blue objects, where abundant, are no longer significant marks of quality. The birds
still collect them , but the y seem to place no more value on them than humans do
on chea p lace.
C H A P T E R
MOVEMENTS AN D
RITUALIZATION
DIFFICULT MOVEMENTS
Male courtshi p movement s ar e ofte n extremel y elaborat e an d difficul t t o per form. Th e super b bir d o f paradise hang s upside dow n o n a branch, flapping its
61
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RITUAL FIGHTING
Much o f th e fightin g tha t goe s o n betwee n rival s o f th e sam e specie s i s ritua l
fighting; the goal is not to injure or kill the opponent, but to convince it and others
that i t i s the weake r an d shoul d withdra w fro m th e contest . Th e initiato r o f th e
fight does not even try to surprise its opponent; rather , it signals clearly that a fight
is imminen t an d let s it s riva l prepare itself ; only afte r it s opponen t ha s assume d
the appropriat e stanc e does th e aggresso r strikeand then onl y a well-protecte d
and "legitimate " target, suc h as antlers.
The horn s o f a male gazelle ar e strong , sharp , lethal weapons. A male gazelle
fighting his rival could surpris e it and run i t through, but h e doe s not. He comes
at hi s opponen t slowl y an d let s it ge t int o positio n befor e locking horn s wit h i t
and pushing an d pounding it in a contest of strength. The end of such a grueling
struggle usually comes when one of the opponent s concedes .
It woul d b e a mistake to cal l suc h a struggle a
fight. I t i s more lik e a competitiv e spor t i n which
contestants tr y t o sho w of f their superiorit y while
following fixed rules. In fact , thes e ar e threats that
take th e for m o f a physica l contest ; th e winne r
does no t pursu e the lose r an d kil l it; it i s satisfied
when it s riva l gives up. I n th e rar e cas e when on e
of th e contestant s dies , i t i s becaus e i t faile d t o
withdraw i n time. 2 Mal e gazelle s hand-raise d b y
humans a s pets treat people as members o f their ow n species, and whe n grow n
up the y may invite their keepers t o a rivals ' contest. Th e keeper , wh o doe s no t
realize that th e gazelle' s initial butt i s an invitation t o ritua l combat , lacks horns
to mee t th e attac k and ma y be fatall y wounded .
The ritua l battles o f ibexes an d bighorn shee p ar e stunning sights. The rivals
rise up o n their hind legs an d hurl themselves with al l their migh t at their oppo nentswho meet the m with a similar charge. The clashe s are repeated again and
again, scores of times. Neither contestan t tries to strike at his rival's body. All his
force i s aimed at and absorbe d by the rival' s strong horns .
These fight s ar e not playacting : they are out-and-out displays of strength an d
agility a t th e en d o f whic h th e contestant s ar e exhausted . I f a n ibe x wishe d t o
finish of f hi s rival , a s a predato r does , h e woul d hav e approache d i t stealthil y
and trie d t o gor e it s bod y wit h hi s horns . Bu t a n ibe x o r a gazell e initiating a
ritual fight approaches slowly and show s off his intentions by lowering his horns.
He wait s fo r hi s riva l t o prepare , an d i f the riva l doe s not , th e challenge r may
butt i t lightl y t o ge t it s attention . B y letting hi s riva l prepare fo r combat , th e
ibex i s takin g o n a handicap ; th e handica p pay s off for th e winne r becaus e h e
convinces hi s immediat e riva l a s well a s an y onlooker s o f hi s superiority . This
saves bot h animal s the ris k inheren t i n a battl e t o th e death , an d on e o r bot h
combatants ma y demonstrat e a prowes s tha t save s it fro m havin g t o dea l wit h
other rivals .
Contests o f force don' t necessarily involve physical contact. Gulls threaten by
tearing up grass, chimpanzees break off branches, rhinoceroses and bulls rake up
dirt with their hooves. Peacocks fan out their tails and hold them upright, shaking
them, which demands a great deal of strength. Since males of these species perform
the same actions, they and others can judge reliably which of the rivals is stronger,
and thus the contestant s are spared a fight.
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66 M E T H O D
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the winner. 7 Thi s seemingl y minute an d trivia l gesture, i n the contex t o f a fight,
means tha t th e fis h i s giving up th e ful l us e o f its gills and i s handicapping itself
by absorbing less oxygen than it can; this is reliable evidence of its stamina and its
chances o f winning the fight . I n nature , just a s in the Olympics , seemingl y negligible differences i n performance can bring about dramaticall y different results . In
the Olympics , th e runne r who come s in first gets a gold medal, while th e on e in
fourth plac e get s no meda l a t all , even thoug h th e differenc e between the m may
be s o small it ca n only be see n with th e ai d of electronic devices. I n th e wild , in
species whose males do not participate in the rearing of young, a very small number
of top performer s get to father most of the next generation, while many males have
no offsprin g a t all.
is watching them, because of their intrinsi c usefulness , rathe r tha n t o conve y any
message. The abilit y to watch fo r specifi c movement s other tha n signal s can then
evolve an d sprea d throug h a populatio n i n th e sam e way that an y other single ,
useful mutatio n does .
Once observer s respon d t o specifi c observe d movements , mutation s tha t exaggerate these movements ma y spread among the ones observed. These mutations
are an advantage to their bearer s because they intensify th e movement in the eyes
of observers wh o already understand its meaning; at this point th e movemen t ha s
become a movement signal.
There i s a cost involved: as soon as a movement becomes exaggerated, it ceases
to be the optimal movement for its original purpose. Still , the investment is worthwhile t o the signaler, who wants to make sure its actions ar e noticed. When a bird
stretches its neck exaggeratedly to ensure that the predatoror birderknows it
has noticed it , it has to stop feeding for the moment and will have more difficult y
in launching itself into flight, since in order t o do so, it would have to pull its neck
back. Bu t th e bir d als o lessens th e likelihoo d tha t i t will hav e to tak e flight and
leave its feeding ground: the potentia l pre y makes it clear to the watcher that th e
watcher ha s bee n spotte d an d tha t approachin g woul d b e a waste of time. Both
bird an d predator gai n from th e signal : the predator ca n save its energy for other,
more vulnerabl e prey , an d th e bir d doe s no t hav e to leav e a feeding o r restin g
spot.
But why do movements that evolve into signals become exaggerated in one way
rather than another? This is where the Handicap Principl e applies. Let's return t o
the wolf-gazell e interactio n tha t opene d thi s book. Eve n befor e gazelle s starte d
signaling to wolves , individual gazelle s reacte d differentl y t o a wolf's presence
they prepare d t o flee according t o thei r confidenc e i n thei r abilit y t o evad e th e
wolf. Wea k individual s fle d righ t away , while confiden t gazelle s coul d affor d t o
stand an d watch the wolf, or even to continu e feeding. In fact , Kruu k describes a
cheetah burstin g into a crowd o f Thompson's gazelle s and catchin g one o f them.
He stresse s that the gazelle the cheetah caugh t was the one who first turned to flee
when th e cheeta h began it s charge. 10
A wol f coul d lear n b y experienc e tha t i t ha d a bette r chanc e o f catching a
gazelle who fle d righ t away . It migh t eve n pa y off for th e wol f t o advanc e more
slowly toward the gazelle s and let them react , so that it could spo t an d chas e the
weaker ones. A confident gazelle can make it easier for a wolfand fo r itselft o
avoid a futile chas e by demonstrativel y postponin g it s escape, or b y exaggerating
movements tha t displa y its fitnes s an d self-confidence , like jumpin g straigh t u p
(slotting). Individual s wil l perform th e signa l differently; their performance s will
differ eve n more than their nonsignal reactions to the wolf's presence, because the
wolf pay s most attentio n to thos e movements that mos t reliabl y demonstrate individuals' differing abilitie s to escape it. It is precisely these movementsthe ones
that prov e t o be reliabl e mean s of communicationthat becam e formalized, ritualized movement signals.
68 METHOD
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Exaggerated movement s use d a s signals are constantly tested by natural selection. The signa l evolves an d endure s onl y as long as watchers gain from i t reliabl e
information tha t is beneficial to them, and a s long as the investment in it is worthwhile t o th e signaler . The benefi t in watching another t o anticipat e its actions is
what generate s movemen t signals ; th e specifi c characte r o f th e movemen t tha t
evolves depend s o n it s specific cost i n th e circumstance s i n which it is used. Fo r
example, movemen t toward a rival became a threat, eve n thoug h sideway s movement would have demanded a s much physical effort an d might have given the rival
a bette r sens e of the detail s o f the movement . I n thi s case , it is the ris k taken b y
approaching th e rival , rather tha n the physical difficult y o f performing the movement o r its specifi c details , that reliabl y displays the degre e of threat .
The standardization and increased difficult y
of movement s use d a s signalstheir ritualizationmakes it easier for watchers to determin e
the difference s amon g displayin g individuals ,
and i n th e reaction s o f the sam e individual i n
different circumstances . I f eac h signale r dis played i n its own way, observers woul d fin d i t
difficult t o compar e them . Movemen t signal s
thus become ritualize d no t s o they can be distinguished from th e functional movements ou t
of which they evolved, but rathe r to enable observers to make fine comparisons among signalers. The logic of movement signals
is the same as that of species-specific pattern s of color and form: uniformity within
a speciesritualizationevolve s ou t o f the competitio n member s o f the specie s
engage i n t o demonstrat e their differences. I n bot h cases , i t i s the observers , th e
ones the signals are directed at , who by their choices drive the evolution o f reliable
and unifor m signals. 11
C H A P T E R6
VOCALIZATIONS
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Vocalizations 7
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RHYTHM
As we saw in chapter 3 , Lambrechts an d Dhondt 9 found that th e more successful
great titsth e one s wh o produce d mor e offspringha d song s tha t containe d
Vocalizations 7
more syllables and were more rhythmical than the songs of other great tits. Among
humans, mor e precis e rhyth m i n threat s tend s t o inspir e greater fear ; i n movies
and o n stage, rhythmic music can announce important o r fearful happenings .
What i s the connectio n betwee n rhyth m and threat ? There is an inherent conflict betwee n collectin g informatio n and precis e executio n o f vocalization. Both
activities demand concentration , but t o collect informatio n on e must concentrate
on listening , looking , discerning , an d correlating , whil e precis e vocalization demands that one concentrate on execution. A person who tries hard to catch a weak
or unclear sound often close s his or her eyes. And many musicians close their eyes,
or assume a dreamy expression, whe n concentratin g o n their playing; they disconnect fro m thei r surroundings.
One wh o trie s bot h t o liste n an d t o vocaliz e i s likel y t o falte r a bi t i n th e
rhythma stumbl e that wil l displa y divided concentration . Therefore , a precise
rhythm show s that one is not collectin g information . One wh o is certain of his or
her ability to win or is determined not to give in does not have to collect additiona l
information. Bu t one less confident, who is still trying to decide which way to act,
needs an y information available. Thi s differenc e between th e confiden t an d th e
wavering is brought ou t reliabl y by a rhythmic threat.10
Anava studie d th e trillin g call s mad e b y babbler s whe n the y mo b perche d
raptors.11 Each trill is composed o f a rhythmic series of short notes an d pauses. A
babbler mobbing without interference from other s tends to make loud, prolonged ,
uniform trills composed o f many syllables. When the mobbing babbler is disturbed
by othe r babblers , however , it s call s ar e affected . Whe n a dominan t bir d ap proaches th e callin g bird , th e caller' s rhyth m is appreciabl y less even . I t i s also
altered, thoug h les s so , when th e mobbin g babble r approache s grou p member s
who ar e subordinat e t o it . The differenc e i s both audibl e t o human s and clearly
visible in recorded analyses (se e Graph 6-1). Interestingly, when babblers get nearest the perched raptor during their mobbing, they fall silent. Apparently, assuming
the mobbing postur e of raised wings and sprea d tai l interferes with the babbler' s
ability to escape swiftly should the perched rapto r try to strike. Thus, the mobbing
babbler canno t affor d t o tak e som e o f it s attentio n of f th e rapto r i n orde r t o
perform vocalizations. Although those mobbing babblers who come nearest snakes
adopt simila r postures, the y make short tzwick calls ; it would see m that snakes are
somewhat less dangerous to babblers tha n perched raptors .
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METHODS O F COMMUNICATIO N
Graph 6-1. Mobbing trills of the male babbler TTZL when alone (a), when disturbed
by the dominant male of his group (b), and when disturbing a subordinate (c). Data
from Anava, 1992. The left side of the graph shows the length of each syllable within
each trill; the right side shows the change in length between each syllable and the one
before it. The difference between states a, b and c may seem insignificant on the left
graph, but when one focuses on the differences, as in the right graph, they stand out
distinctly. Again, these differences are clearly audible to the human earnot to
mention to other babblers.
terns; so does the need to make a call loud enough to be heard over great distances.
The differences tha t high volume does not conve y well are often th e very ones that
the cal l i s mean t t o communicate . Fo r tha t reason , voca l communicatio n ove r
distance usually consists of a series of syllables, and rhythm and changes of volume
convey a great dea l of the information. Such a series also gives the listener tim e to
locate th e sourc e of the sound , tur n t o it, and thus better perceiv e fin e variations.
Indeed, Katsir showed tha t babblers' calls vary according t o the distance they are
meant t o cover: the greater the distance, the more constan t the frequency and the
greater th e variations in syllable duration. 12
WHY SHOUT ?
It isn' t alway s easy to tel l just whom a vocal communicatio n is directed at . As we
noted already , the discrepancy between the loud "warning calls " a sentinel babble r
makes and the short distance between th e sentinel an d other members of the group
led us to understand tha t the calls were actually aimed at the distant predator. But
sometimes babblers make loud calls even when clearl y communicating with other s
nearby. Humans, too , sometime s shout a t nearby listeners.
Everyone know s tha t ther e i s often a correlation betwee n volum e an d th e de -
Vocalizations 7
gree of anger or of a threatthe louder the shout , the more intense the ange r or
threat. We suggest 13 tha t i n these cases too th e shoutin g is aimed not a t the purported listene r bu t rathe r a t othe r babblersor humanswh o ar e farther awa y
and ar e no t partie s t o th e conflict . Th e shoutin g make s the m witnesses . Whe n
someone threaten s anothe r i n private an d the n doe s no t carr y out th e threat, he
or sh e loses standing i n the eye s of that person only . When other s are made witnesses, failure to carry out the threat will cause the threatener to lose standing not
only i n th e eye s of th e on e threatene d bu t als o i n th e eye s of th e witnesses . By
shouting, the threatener raise s the stakes and makes the threat more reliable; only
confident individual s ca n affor d t o shou t thei r threat s befor e th e crowd . Thi s
principle is well-known i n politics: a publicly declared intention is likelier t o b e
carried out tha n on e agreed upon i n secret .
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MIMICRY
It i s fairly commo n for animals and especiall y for birds to mimic the call s of other
individuals or other species and even background sounds. Payne16 and McGregor17
Vocalizations 7
found tha t bunting s an d tit s mimi c the song s o f their neighbors ; mimickin g by
singing crested larks in Hatzeva have often caused us to stop and look for babblers,
and a friend of ours often ran needlessly to the phone, deceive d by the mimicking
of a jay. The top marks in mimicking belong t o parrots and mynas, who can mimic
human voice s an d us e word s an d sentence s i n appropriat e circumstances. 18 I t
would b e fascinating to study the use and value of the imitative faculties of parrots
and mynas in the wild .
It seem s tha t mimicr y fulfills severa l functions. On e i s to convinc e a listene r
that the communicatio n is addressed t o it specifically, a s we saw in chapter 1 . Ofer
Hochberg19 tol d u s of a jay near hi s house that would cal l like a cat when i t saw
a cat. Alan Kemp of South Afric a severa l times observed a drongo tha t mobbed a
Wahlberg's eagl e whil e utterin g mimicrie s of th e eagle' s call s mixe d i n wit h it s
own alar m calls . The drong o nea r Kemp' s hom e kne w th e call s of several hawk
species an d woul d mimi c them correctl y when the y passe d by. 20 I t ma y be tha t
both drong o an d ja y were tryin g to convinc e thes e predator s tha t the y had see n
them specifically.
Birdsong, amon g its other functions, proclaims th e singer's readines s to defen d
its territory. By mimicking a neighbor's song , a singer addresses its threats to that
neighbor i n particular. Tits, nightingales , and th e male s of many other territoria l
bird species often mimic the rival they are addressing.21 As they grow older, males
of many species, such as the lyrebird, the bowerbird,22 an d the nightingale, expand
their repertoir e of mimicked sound s an d o f songs. It ma y well b e tha t thei r eve r
more variabl e mimicr y let s the m sho w of f their experience , their age , an d thei r
ability to learn an d remember . Humans, too, mimic sounds extensively, and Darwin sa w in thi s abilit y th e foundatio n o f th e abilit y t o speak. 23 W e believ e tha t
mimicry still plays an important role in human linguisti c changes suc h a s shifts in
vowel sounds, the adoptio n o f new words and phrases, changes in the meaning of
existing words, and the like.
78 M E T H O D
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Vocalizations 7
8O M E T H O D
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dangers: many animals reac t appropriately even to the calls of other species, whic h
are clearl y not directe d a t them. Bu t we d o no t thin k tha t suc h call s evolved for
the purposes o f letting others know the enemy' s identity.
It i s well known tha t animals can correlate thing s with specific sounds, including words. This ability is used by trainers who teach animals to perform in response
to commandsto words. Th e trainer teache s the animal to understand fragments
of his or her word language. Dogs, dolphins, and parrots can learn persons' names
and ca n o n comman d sit , stand , tur n lef t o r right , fetc h specifi c item s an d pu t
them in specific places. Some animals can understand simple concepts encoded in
words, and can make specific sounds on command. Why, then, did they themselves
not evolve a language of words, as humans did, to describe t o their partners where
exactly food is located, to alert them to anticipated dangers that are not yet present,
or to convey an y other information tha t is best expressed by words?
In the final chapter we will discuss the special nature of
human language, its strong points, and its drawbacks. Here
we shall only say that, with all its potency, human language
has n o componen t tha t guarantee s its reliabilit y an d pre vents cheating; nor is it in and of itself well suited to convey
exact, fine gradations of feeling and intention. Thus , in no
human society does the language of words replace wordless
communicationcommunication by nonverbal sound, intonation, stance , and movements. And this wordless, nonverbal communication is the onl y "speech" of animals.
C H A P T E R7
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82 METHOD
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combs an d danglin g facial flesh:3 fighting cocks raised by humans were suppose d
to kil l thei r rivals , not dete r the m wit h effectiv e threats . A cock without a com b
may be able to fight better, but a s it cannot threaten reliably, it cannot win without
a battle .
The tail s of many birds, such as swallows and terns, have extralong feathers at
the edges (outer tail feathers); in such birds as bee-eaters, yaegers, and tropicbird s
these displa y feathers are in the center o f the tail. They are usually longer i n males
than i n females, and longe r i n older male s than in younger ones. Fo r th e matin g
season, the male widowbird, a sparrow-size songbird of the savannas of East Africa,
grows tail feathers a foot and a half long.7 A widowbird displayin g in flight abov e
its singin g post look s lik e a long, black, waving ribbo n wit h a small bulge a t th e
frontthe bod y of the bird . Mal e widowbirds, lik e peacocks , have to bear suc h
extreme handicaps because they do not participate in rearing the young: their only
contribution to the nex t generatio n is thei r sperm . Thus , female s do not min d
sharing them with others and can afford t o search for the few most superior males,
who end u p fathering mos t of the next generation.
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with vision in some plovers and in Cracidae, large birds that gather fruits from th e
tops o f tropica l trees . Asiati c hornbills liv e a t th e to p o f tropica l forests . Thei r
gigantic bill s ar e adapte d fo r pickin g fruit fro m th e en d o f branches. Bu t som e
have large horny cask s on their beaks , almost like anothe r beak , which overhang
their eyes. The cas k impairs their ability to see birds of prey flying above and their
ability to peck efficientl y a t fruit righ t in front o f them, and als o adds unnecessary
weight to the beak.
Bustards are large fowl o f the ope n deser t an d savanna . The neck o f the male
is covere d wit h lon g feathers ; when h e displays , he stretche s his nec k fa r backward, an d hi s nec k feather s stand up , formin g a large ball. H e canno t se e what
is aroun d hi m an d dance s blind . Onl y a mal e secur e i n hi s knowledg e o f hi s
surroundings an d confiden t in his abilit y to overcom e predators an d rival s alike
can affor d t o danc e fo r minute s a t a time without bein g abl e t o see , in ful l vie w
of al l comers. In fact , the bustard's blind dancing might b e too great a handica p
for i t to bea r i n environments other tha n th e ope n flatland s i n which it lives; the
specimen a t th e Te l Avi v University zoo repeatedl y bumped int o it s fence whil e
displaying.
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off signal . In human s and i n som e monkeys, noses sho w the directio n o f an individual's gaze. The nos e is more develope d i n males than i n females, an d mor e in
adults than i n th e younga n indicatio n o f its use fo r showin g off. Small tufts of
feathers o n bot h side s o f the head , a s in owls an d othe r birds, an d shor t horns ,
such as the bony protrusions on the heads of giraffes, als o let an observer see from
afar whic h way the animal's head is turned.
The arche d horns of gazelles, antelopes, and other suc h animals also show off
the directio n o f their gaze ; we found tha t ou t a t the Shushlu i Nature Reserv e in
South Africa. Till then we had always toured African reserves by car. At the Shushlui, a student doin g researc h offered Amot z a chance to sightse e on foot. Unpro tected and unarmed among lions, rhinoceroses, and buffaloes, Amotz couldn't hel p
but liste n t o ever y sound an d kee p a constan t watc h o n hi s surroundings . Th e
animals were no t use d t o th e sigh t o f humans walking; antelope s barke d a t th e
sight. Becaus e of the distance , neithe r thei r eye s nor eve n th e marking s on their
faces coul d b e seen, but thei r horns always looked eve n and distinct to Amotz and
his guid e an d followe d the m around , proo f tha t th e antelope s were lookin g a t
them.
The rea l adventur e o f th e tou r cam e i n a n encounte r wit h a square-lippe d
rhinoceros. Square-lippe d rhino s have two horns: the larg e frontal hor n serve s as
a weapon; Amot z had a hard time trying to figure out th e function of the secon d
smaller horn behind itunti l the rhin o cow charged.
The guide had assure d Amotz that square-lipped rhinos are usually peaceful, and that even if they charge, one
can usuall y deter the m a t th e las t minute , o r escap e be hind a tree. They came within a hundred yards of a rhino
cow and her young calf. The guide, who probably wanted
to sho w off , suggeste d gettin g nearer . Amot z ha d n o
choice bu t t o com e along ; being lef t o n hi s ow n was an
even more frightening prospec t than the rhinos.
The rhinocero s co w snorted, stamped , an d charged .
Amotz an d th e guid e clappe d thei r hand s to dete r her ,
and indeed at about twenty yard s she swerved aside. The instant she turned, the
small horn coul d be seen : unti l then it had been hidde n behind th e large, threatening fronta l horn . I t was only then tha t it became clea r that th e functio n o f th e
rhino's smaller hor n i s to show what direction its owner is facing.
The smal l horn lets one tell whether a rhinoceros i s confident or hesitating. A
rhino with a well-developed back hor n canno t hide it s intentions; an y hesitation,
any change of direction or glance sideways i s unmistakable. Such horns function
this way only in an open landscape , where they can be see n fro m afar . Th e horns
of Asiatic rhinos, which live in dense vegetation, do not sho w the directio n of the
rhino's gaz e in a similar manner, and indee d thei r bac k horn s hav e degenerate d
into small horny bumps.
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88 M E T H O D
S OF C O M M U N I C A T I O N
goats an d ibexe s ar e not efficien t fightin g weapons . I n fact , Darling 14 note s that
the lunge of an antlerless deer is far more dangerous than that of an antlered deer.
Yet it is clear that the larger and more branched a deer's antlers, the more attractive
they are to females and the more of a deterrent t o other males. 15
From tim e to tim e on e finds deer withou t antler s (hummel ) or with straight
antlers (pronghorns) . Darling remark s tha t i n battle , straight , sharp antler s ca n
wreak a great deal of harm. But such deer disappear from natural populations: the
straight antlers may be better weapons but ar e less effective when used to threaten
and to display one's strength. It may well be, then, that heavy, cumbersome horns
and antler s evolved no t simpl y as weapons, but rathe r a s handicaps that show off
the strength of the animals that carry them. Females see m to be looking for males
that ar e stronger overall, not fo r males who ca n kill better.
in regular , nondisplay flight . I n eithe r case , cuttin g of f some of the win g feathers
surely affects the displays flights but proves nothing about the purpose of the larger
wings of male skylarks.
9O M E T H O D
S O F COMMUNICATIO N
better indicator s o f each male' s overall quality, and bette r instrument s for ritua l
fighting, eve n though the y are less effective a s conventional weapons .
Changes occurring in this later stage of signal selection were confined to males:
Females, a s we have seen, have to inves t more i n eac h of their offsprin g tha n d o
males, since eggs are larger and fewer than sperm; female mammals have to invest
even mor e i n pregnanc y an d suckling . Thu s the y have less to inves t i n showin g
off. The y als o have less to gain : the numbe r o f offspring eac h female can bear in
her lifetim e is far more limited, whereas the numbe r o f offspring a male has de pends far more on the number of partners who mate with him. Thus females have
to g o fo r qualit y an d concentrat e o n carefull y choosin g th e father s o f thei r offspring. Of course, thi s means that males are much likelier tha n females to end u p
with no offsprin g at all. Thus male s show off considerably more than females do ,
particularly whe n th e female s d o no t nee d thei r hel p i n raisin g offspring . Thi s
explains the great size and weight of male horns, and the wealth of complex shapes
they take ; by contrast , females, when horne d a t all , ten d t o hav e small , sharp ,
efficient horn s for protection agains t predators.
But a further interestin g stage in the evolution of antlers occurred in reindeer :
their heavy , branching antlers evolve d a n extra branch, which turned ou t t o be a
useful too l fo r clearin g snow of f the lichen s the y eat i n winter . This i s probabl y
the reaso n female reindeerunlike other femal e deergro w antlers.
The evolutio n o f horns an d antler s thus consiste d o f several alternating stages
of natural selection. Originally, structures that signaled the direction o f an animal's
gaze evolved by signal selection, an d their shap e and position wa s determined b y
this function. These structure s became progressively stronger , evolving by utilitarian selection int o weapons. They continued t o change, becoming larger and more
elaborate a s the y evolve d int o handicap s an d instrument s o f ritua l rathe r tha n
actual combat . An d wit h reindeer , antler s furthe r develope d int o food-findin g
tools. Still, throughout the saga, in all their various permutations, horns and antlers
continued t o serve as signals that showe d the directio n o f an animal's gaze.
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C H A P T E R
94 ME
T H O DS O F C O M M U N I C A T I O N
BLACK I N TH E DESER T
The first inkling we had that there might be a logical reason tha t a particular bird
was a certai n colo r cam e fro m a pape r publishe d i n 195 0 b y tw o outstandin g
ornithologists, May r and Stresemann. 3 They pointe d ou t tha t wheatears living in
open habitats , such a s the desert wheatear and the isabelline wheatear, are cryptic
in coloring, while wheatears that live in hilly country and inhabit deep gorges, such
as the mournin g wheatea r an d th e white-crowne d blac k wheatear , have conspicuous black and white coloring. They also pointed ou t that the tails of species living
in open habitat s tend to be black, while the tails of those living in mountains have
more white in them .
We soon notice d tha t othe r deser t bird s ten d t o have black body parts tha t in
birds of more temperate habitats are usually white: skylarks have white on the sides
of thei r tails, while th e side s o f desert larks ' tails ar e very dark (thoug h not quit e
black). The Cretzschmar' s bunting in the Mediterranean area s of Israel has white
tail feathers, while the deser t buntin g ha s no white in its tail.
This rule applies to desert mammals as well. Male ibexes have huge black horns
and blac k beards , bot h ver y conspicuou s agains t th e beig e backgroun d o f th e
desert; sometime s th e black horns an d beard ar e the only clu e to the presenc e of
this otherwise ver y cryptic animal. During courtship , th e male ibex grows magnificent black fur on its chest. Black shows up clearly in the desert in all lights, except
for th e ver y rare cases in which the deser t backgroun d itsel f is very dark. Black is
more clearl y visible than any other colo r eve n in the middle o f the day , when th e
hot air blurs one's vision. At dusk, when the gray body of a blackstart merges with
the twilight , the spreadin g black fa n of its tail can still be seen .
In the desert s o f the Nege v an d the Sinai , the black garment s and black goats
of the Bedoui n ar e conspicuous from fa r away; it occurred to us that this conspicuousness might be precisely the reason these people wore black clothes an d chose
black goats . Whe n we mentioned thi s ide a to researcher s who stud y the physiological connection betwee n color s an d temperatures, the y smiled an d pointed ou t
that i n th e Sahara , the Bedoui n dres s i n light colors ; wouldn' t thi s indicat e that
the Bedouin selec t th e colo r o f their clothin g arbitrarily?
When peac e with Egyp t allowe d u s to visit th e Western Desert , th e Egyptia n
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the greatest contras t with most backgrounds, it shows these birds' shape s to perfection. Th e blurrin g o f the edge s o f white bodie s ma y explain wh y hardly any
small bird s ar e completel y white. Presumably , such birds a s swans or egret s ar e
large enough that a minor blurring of their outlines is insignificant fo r them.
White is especially effective in advertising movement: a soaring flock of pelicans
or gulls is revealed b y the light reflected off the white patches on their wings and
bodies a s the y turn . Th e reflecte d ligh t ca n revea l speed , win g movement , an d
other factors . I n fact , man y birds have white in their wings or tails that i s visible
only when the y are i n flight. The blurrin g cause d by white i s not a n issu e here,
since these birds' motio n itself blur s their outlines .
In Australia , we visited friend s whos e daughter came
home cryin g fro m he r firs t balle t lesso n becaus e th e
teacher scolded he r fo r not wearin g the traditional black
leotard. The teacher explained tha t without the black leotard, the exact position and line of the girl's body could
not b e see n a s clearly and s o were harder to correct . I n
performance, o n the other hand, ballet dancers are more
likely to b e attire d i n whit e o r i n ver y ligh t colors : thi s
increases the audience's ability to appreciate the dancers'
movements rather than isolated positions .
97
natural habitat it is actually cryptic and conceal s the bird agains t the gree n background o f the forest .
The influenc e of environmen t o n th e selectio n o f colo r ma y explai n a phe nomenon note d b y Diamond 4; mixed-specie s flock s o f bird s i n tropica l forest s
are usuall y made u p o f specie s tha t hav e simila r colors . H e describe s flock s o f
birds who are mostly black an d brown o n the forest floor; green and yellow birds,
mostly insect-eaters , wander te n t o twent y feet up . Eac h suc h flock roam s a certain leve l o f the jungle , and w e think the birds ' color s sui t th e par t o f the fores t
in which they are active: the to p o f the canopy , halfway down , or the forest floor.
Since bird s o f whatever specie s o n a give n "story " hav e t o dea l wit h th e sam e
conditions o f light an d distance , they use simila r colors .
We find the same pattern amon g fish. In open water most
fish are gray , black , o r white ; o n th e cora l reef s an d i n kel p
forests, wher e long-rang e visibility is obscured an d shadow s
and patches of light abound, bright colors enable fish to show
off a t shor t range.
Once we figured out thes e "rules, " we made up a game,
using the description s o f birds' color s in guidebooks to guess
the habita t an d som e o f th e behaviora l traits o f specie s un known t o us . When w e compare d ou r prediction s wit h th e
knowledge o f local birders, we usuall y found a good match.
We wer e therefor e surprise d when tol d tha t th e golde n bowerbir d display s near
the groun d i n th e dee p rai n forest . W e woul d hav e expected thi s bright yello w
bird t o displa y in the well-lit upper part s of the green canopy.
Fortunately, we were able to visit Gerald Borgia at his study area near Atherton,
Australia. We waite d fo r a long tim e in blind s nea r th e bowe r o f a golden bow erbird, hearing its calls without seein g it . Suddenly the bowe r was lit by a ray of
sunlight. Th e mal e cam e flying down th e sunbea m a s though h e wer e par t an d
parcel of it, and landed on his perch, a horizontal branch joining the two pyramids
of stick s tha t mad e up hi s bower. Th e ligh t was reflected ont o th e bir d b y light
gray lichens, whic h he ha d place d o n th e sam e branch. Th e bowerbird' s golde n
color now made sense; but ho w could sunligh t penetrate tha t deep into the fores t
floor? W e late r learne d tha t mal e golde n bowerbird s meticulousl y pick of f th e
leaves above their bowers t o let the light penetrate at the angl e they desire.
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METHODS OF COMMUNICATION
body that are seen while the bird is perching are most often black ; white and light
colors ar e ofte n hidde n whe n th e bir d i s at res t an d reveale d onl y when i t i s in
flight. Som e species, though, have markings o f both colors that can be seen when
the bird i s at rest. This allow s the bird t o advertis e in all lights: the white belly of
the great gray shrike and of the wheatear glisten in the light when the sun is at the
observer's back , but whe n the bird is perched between th e sun and the observer ,
the blac k a t the sid e of its wings helps defin e it s outline. Sometime s the messages
are aime d onl y at nearby observers: the zebra' s stripes, which accentuat e bodily
features, merge into a cryptic gray at a distance.
Two contrastin g color s o n a bod y reduc e th e
overall impression it makes and the distance at which
its shap e ca n be see n distinctly ; it ma y also distor t
the overal l shape . Fo r tha t reason , w e ofte n fin d a
"compromise color" : on e tha t i s dar k enoug h t o
show the animal' s shape, yet reflects mor e light than
black o r dar k red . I n ope n habitat s an d abov e th e
forest canopy the most common compromise color is
gray; insid e th e fores t i t i s mostly beige, orange , or
brown. O n th e forest floo r one finds a great dea l of
reddish-brown, whic h i s th e colo r o f man y fores t
mammals includin g squirrels , the commo n re d do g
of India , an d th e sambar , a n Indian fores t deer , all
of whom liv e in th e depth s o f the jungle . The sambar's undertail "flag" is light brown, unlike the white "flag" of deer in open spaces.
Another recurring pattern is the presence of two similar but not identical colors
to advertise one message over a short distance and another over long distances. A
nearby observer sees the details; over distance, both colors merge into one message.
The distance that the detaile d message travel s varie s wit h th e siz e of the patche s
of colo r an d wit h th e intensit y of the contrasts . Th e dar k re d patc h o n the red winged blackbird's wing is very prominent a t close rang e but doe s not lessen th e
effect o f the bird's silhouett e when it is seen from a distance.
99
EXCEPTIONS TO TH E RULES
There are exception s to the rule s we hav e outlined : bee-eater s and roller s are
colorful bird s tha t live in ope n habitats ; many finches an d bunting s (calle d sparrows in the Ne w World) tha t live in open habitat s ar e red an d yellow , and ther e
are black and white flycatchers that live in woodland an d forests. Once one knows
the bird, an d what its habitat is like in all seasons, however, one can often explai n
such exceptions . Fo r example , th e yellow-bille d finc h (Melanoderma xanthogrammd] tha t lives in open habitats in the Patagonian Mountains of South America
has a black chi n wit h a yellow outline, rathe r tha n a white outline, a s one might
expect a bird living in the open to have. Watching the finch in early spring, when
the birds arrive to stake their territories, however, we realized that at that crucial
time the bird s often stoo d and san g on rocks where there were many patches of
snow. Whit e woul d hav e bee n les s effectiv e agains t suc h a background; yello w
worked muc h better . A relate d species , M . melanoderma, whic h live s a t lowe r
altitudes, below the sno w line, has a black chin outlined wit h white.
Another example: the black and white flycatchers (Picedula spp.) arrive at their
breeding grounds when many trees of the forests and woods are still bare of leaves.
A close r look a t the place s i n which the y display may well sho w that a t the star t
of breedin g season , when effectiv e displa y is crucial , th e ligh t i n thei r habitat i s
similar t o tha t o f open countryeve n thoug h the y are forest birds ; thus th e us e
of black an d white .
Another possibl e complicatio n i s th e effect s o f ultraviole t light , t o whic h
some bird s ar e sensitive , unlik e humans. 3 I t i s ver y possibl e tha t som e color s
look differen t t o bird s sensitiv e to U V tha n the y look t o us . Thi s ma y explai n
the color s o f kingfisher s an d bee-eaters . O n th e othe r hand , th e amoun t o f UV
light i s usually minimal, especially in forests . This subject requires more detaile d
research.6
The hypothese s presente d i n thi s chapte r ar e base d o n ou r
subjective impressions of the birds we watch. Still, the search
for logica l explanation s regardin g the color s of particula r
birds an d animals has taught us to see their lives and habitats
with new eyes. Our observation s tend to raise questions other
than thos e deal t wit h i n most studie s o f color , an d w e hope
our suggestion s will lead to new and fruitfu l research .
C H A P T E R 9
CHEMICAL
COMMUNICATIONS
any organisms, bot h mono- and multicellular, communicat e by secreting chemica l molecules and mak e decisions based o n chemica l molecules secreted b y others. Suc h chemicals , which are produced b y one
individual an d influenc e th e action s of othe r individuals, are calle d pheromones.
In order to carry reliable messages, pheromones hav e to meet the three conditions
we have established fo r signals : they have to b e costl y to th e individua l sending
them; th e cos t ha s to be more of a burden t o a dishonest communicato r tha n t o
an honest one; an d ther e must be a logical relationship between the specifi c cos t
of the signal and the message conveyed by the signal .
1O2 M E T H O D
S O F COMMUNICATIO N
Chemical Communications 1O
one canno t distinguis h amon g them? Indeed, Elli s an d hi s colleagues foun d tha t
female cotto n leafwor m moth s who were placed in an environment high in female
pheromones stoppe d reactin g t o mal e courtship ; th e numbe r o f copulation s fel l
almost t o zero. 3 Mal e activity , o n th e othe r hand , wa s increase d unde r simila r
conditions.4
What i s the connectio n betwee n th e secretio n o f female pheromone s an d th e
quality of the female? It may well be that a female who is better able to manufacture
new membranes to replace thos e impaired by the pheromones ca n therefore affor d
to secret e more pheromones . I t ma y also be that th e abilit y to replac e membran e
is correlated t o th e fa t reserves in a given female's body, which i n turn correlate s
with her abilit y to lay eggs. In tha t case , the productio n of more pheromones, or
of pheromone s wit h a higher concentratio n o f active molecules, would testif y re liably to the female' s ability to lay eggs, making her desirabl e t o males.
The evolution of female pheromones probabl y parallels that of any other signal:
to begi n with , female s secreted variou s fatty acid s o r relate d fatt y substance s o n
the cuticle, like many other organisms. These chemicals were costly to a greater or
a lesser degree , partly because of the damag e they inflicted o n living cells; but th e
protection the y offered wa s worth th e cost . Still , th e amount s each female coul d
afford t o secret e woul d vary , and i t is reasonable t o assum e that there was a correlation betwee n th e quantit y of these chemica l secretions an d th e qualit y of th e
female secreting them. Quite likely, males evolved receptor s sensitive to the chemical mixture s tha t bes t reflecte d a female's quality. (Thi s would b e analogou s t o
the "mind-reading " i n the developmen t o f ritualization, at which stag e observers
note functional motion s or postures that precede certain actions but which are not
intended t o signa l thos e actions. ) Onc e tha t happened , the n mutation s causin g
overproduction o f these chemicals would benefit their bearers. At that point, signal
selection took over, and picked a s pheromones th e chemicals that impose the most
telling handicaps and thus provide th e most reliable information about th e quality
of th e female.
Although there is a great deal of similarity between th e pheromones o f females
of various species, each species has its own special mix of chemicals, which can be
used to identify it. The male's brain has receptors adapted to the specific chemicals
typical of a female o f his species; a few molecules of chemical are enough to cause
a reaction i n the male's brain . This would see m to support th e idea that the pheromones evolve d i n orde r t o identit y the specie s o f the female , bu t w e think oth erwise. Afte r all , th e female s themselve s hav e receptor s tha t reac t t o chemical s
secreted b y the plant s the y lay eggs on, plant s that thei r offsprin g consume ; yet it
is highly unlikely that the plant s secret e the chemical s in order to announce thei r
presence an d their identit y to their pests !
We thin k that th e typica l mix of pheromones fo r eac h species is a by-product
of th e species ' ow n distinctiv e metabolism . We ca n draw an analogy to alcoholi c
beverages that humans consume. Each nationality has its characteristic drink: Russians typicall y imbibe vodka ; Serb s prefe r slivovitz , and Japanes e lik e sake . But
1O4 M E T H O D
S O F COMMUNICATIO N
nobody claim s that th e various alcoholic beverages evolve d s o that the nationality
of their consumers could b e determined. Rather, each develope d ou t o f a people' s
simple desire fo r a n alcoholic beverage . The specia l characte r of each beverage is
a by-produc t o f th e differenc e i n th e ra w material s an d technology availabl e in
each culture. 5
The specia l physiology and die t o f each species , then , affect s th e compositio n
of the femal e pheromone s o f each species . Bu t tha t substanc e evolves as a pheromone i n th e sam e way that othe r signal s evolve : i t deliver s a message about th e
genuine qualit y of the individual that secretes i t in a way that cannot be profitably
faked. We assume that male moths choose their mates according to females' ability
to secrete harmfulthat is , handicappingcomponents of their pheromone. Ob viously, as in other case s of selection, moth s do not rel y solely on the compositio n
of pheromone s t o choos e amon g candidates ; othe r factors , suc h a s the rat e an d
timing o f pheromone emission , an d th e female' s movements, probably affec t th e
final selection o f one femal e ove r another .
Chemical Communications 1
05
The fac t tha t yeast s select thei r mates rather than matin g at random supports
our assumptio n tha t eac h organis m advertises its quality, rather tha n its identity.
But we doubt tha t the amount of peptide constitutes a reliable test of quality. The
short peptid e tha t comprise s th e pheromon e i s not a harmfu l chemical ; it s raw
materials ar e readil y available; and ever y yeast cell i s genetically programmed t o
produce i t an d supplie d wit h th e necessar y information. The proces s o f protei n
production in the cel l is an ongoing one, an d the pheromone peptid e constitutes
only a minuscule part o f the yeas t cell' s output .
Thus, i t is hard to imagine how a short, simple peptide ca n reflect th e pheno typic quality of the advertisin g cell. In addition , the concentratio n o f a chemical is
not a goo d indicatio n o f quality , since a nearby cel l producin g smal l quantities
would b e perceived a s equal to a more distant cel l producing much higher quantities. S o we starte d lookin g fo r indication s tha t other molecule s ar e involved in
the communicatio n betwee n yeasts , molecule s tha t ca n testif y t o th e phenotypi c
quality of the cel l by means other than shee r quantity.
It turned out, when we surveyed existing literature, that the yeast pheromone
the peptideis cleave d ou t o f a larg e protei n molecule , calle d a propeptide o r
propheromone. Th e propeptid e o f the alph a gende r i s a glycoproteina protei n
that carries sugars. We believe tha t glycoproteins are better suite d to testify to the
quality of a cell than simpl e proteins , or peptides. Unlike the manufactur e of the
amino acid backbone of proteins, all of which are produced by the same enzymatic
machinery, the synthesi s of the specia l sugars of glycoproteins occurs by means of
special enzymatic pathways that are activated only under specific conditions, which
depend o n th e physiologica l state o f the cell . Fo r example , i n human s th e composition o f th e variou s sugar s on th e gonadotrophi c hormon e FSH , whic h i s a
glycoprotein, varies with change s in the female menstrual cycle.8 The compositio n
of sugar s on a give n glycoprotei n an d th e numbe r o f unit s o f suga r vary . Thi s
microvariation, a s it i s termed, ca n reflec t specifi c condition s i n a way that pur e
proteins cannot . I n othe r words, the complemen t o f sugar units on a specific glycoprotein ca n reflect reliabl y the conditio n o f a cell.
In yeasts , it turns out tha t th e alph a propheromone i s essential to the proces s
of mating , not jus t necessary to the manufactur e of the pheromone : i n lab experiments, yeas t cells that ar e manipulated s o that the y can produce th e alph a pro pheromone bu t los e the abilit y to cleav e the pheromon e fro m i t ca n still mate, if
pheromone is added to the mixture ; but whe n scientist s prevent yeas t cell s fro m
producing the propheromone, th e cells cannot mate even if supplied with the alpha
pheromone.9
Two genes produc e alph a propheromone, an d eac h produces a different version: fou r molecule s o f pheromon e ar e cleave d fro m on e versio n o f th e alph a
propheromone; a n identical pheromone molecul e and one that is slightly different
are cleave d fro m th e othe r version . Al l natural population s o f yeasts have both
genes, eve n thoug h th e pheromon e cleave d ou t o f th e tw o version s o f th e pro -
1O6 M E T H O D
S O F COMMUNICATIO N
pheromone i s nearly the same . It would see m that the orde r an d number o f molecules o f pheromone i n eac h of the tw o variants of the alph a propheromone are
essential an d important, not accidental .
What i s the rol e of the alph a propheromones i n the communicatio n that precedes mating between yeast cells? One en d of the propheromone ha s a hydrophobic segment a segmen t tha t dissolve s i n fats , bu t no t i n water . Th e other en d
contains the pheromon e segments . The sugar s of the glycoprotei n ar e connecte d
to a middle segment. The pheromone segment s are cleaved off the propheromon e
by enzymes and are secreted by the cell. The pheromone molecules reach the other
gender, ar e sense d b y its receptors, an d trigge r the receivin g cell int o sendin g a
copulating offshoo t towar d th e cel l secreting the pheromone .
There is indirect evidence that complete molecules of the propheromonethat
is, propheromon e wit h it s pheromone segment s still attachedca n b e foun d on
the outer membran e of the yeast cell that secretes the pheromone. Ou r conjecture
is that th e alph a propheromon e i s anchored t o th e cel l membran e by its hydrophobic segment in such a way that the pheromone section s attached to it protrude
outside th e cel l membrane, and tha t the y are held i n a specific spatia l configura tionin which the sugar s in the middle segmen t of the molecule probably play a
role.
We thin k tha t these pheromone segment s may bind t o receptor s i n the othe r
cell's offshoot , jus t a s free pheromon e does . I t may even be that both type s of the
alpha propheromon e are needed for a good link : a bond form s betwee n the two
alpha propheromones ( a heterodimer), an d then thei r peptide s link with a group
of receptor s o n th e membran e of the receivin g cell. This woul d explai n why the
pheromone i s manufactured by tw o gene s rathe r tha n one . I t make s sense tha t
impairments i n th e geneti c o r phenotypi c qualit y of th e advertisin g cel l woul d
affect th e number o f sugar molecules attached to the propheromone an d thus the
spatial configuration of the propheromone i n that particular yeast cell's membrane.
A change i n th e spatia l configuratio n coul d wel l affec t th e strengt h o f the bon d
between th e propheromone s o n the signalin g yeast cell and th e receptor s o n th e
other yeast cell, and thus affect mat e preference: an individual cel l weakly bonded
to its would-be partner might detach itself to bond strongl y to a preferred mate.
If this conjecture proves true, then the role of the pheromone peptide itself a
relatively small, mobile moleculewould be merely to draw the attentio n of cells
of th e othe r gende r to the cel l that secrete s it, so that the y would com e an d "in vestigate" by sending a mating offshoot towar d it s membrane. The critica l "deci sion" whether to go ahead and mate with that particular partner would b e based
not o n th e pheromon e bu t o n contac t betwee n th e propheromon e o n th e
membrane of the one yeast cell and the receptors o n the other cell' s membrane.
We hav e describe d ou r interpretatio n o f th e communicatio n betwee n yeas t
genders in detai l because we see it as a general model: i t illustrates how cell s can
advertise their phenotypic quality by means of peptides an d their propeptide pro genitors, which hold them in specific spatial configurations. Indeed, recent findings
Chemical Communications 1
07
show that the propeptides of other peptide s used in communication als o bond to
the sam e receptors t o which the peptides themselve s attach.10
We believ e tha t mos t i f not al l chemical communicatio n betwee n individual s
contains reliabl e testimon y about th e phenotypi c qualit y of the on e sendin g th e
signal. Molecular structures ca n serve this purpose no less than bodily adaptations
do i n highl y developed organism s suc h a s mammals and birds . Needles s t o say,
we do no t clai m that yeasts make conscious decisions ; bu t th e proces s o f natural
selection sa w to it that individuals who followed better lif e strategies, by means of
whatever mechanisms, survived and multiplied, while those who did not perished.
1O8 M E T H O D
S O F COMMUNICATIO N
wrong phenotype. In other words, we find a use for the Handicap Principl e withi n
the multicellular body.
It was recently foun d that free radicals lik e nitric oxide and carbon monoxide,
which ar e very poisonous, ar e used i n communication between cell s in the bod y
and ar e secrete d b y nerv e cell s i n importan t bod y part s lik e th e brai n an d th e
heart.12 Thi s us e o f highl y toxic chemical s i n th e mos t crucia l bodily messages
supports ou r view . O n th e othe r hand , the fac t tha t man y hormones an d many
neuropeptides tha t conve y signals within th e brai n ar e shor t peptide s seem s to
contradict the Handicap Principle: a s we said in the discussio n of yeasts, we don't
think that short peptides have the capacity to provide reliability in communication.
It ma y be, though , tha t i n a t leas t som e o f th e peptid e signal s in th e body ,
reliability i s provided not by the short peptide itself bu t rather by the prohormone
(propeptide) t o which it is attached. 13 The propeptide , i n other words, may well
provide reliabilit y i n th e sam e way that w e sugges t th e propheromon e doe s i n
communication between yeas t cells.
Another metho d fo r ensurin g reliabilit y in signalin g is used, i t seems , in th e
EGF system . EGF i s a peptide tha t enhance s the divisio n o f cells in the wall s of
blood vessels . Thes e cell s divid e whe n a damage d blood vesse l need s repair . I t
turns out that EGF causes cell s to divide only when it is attached t o special sugars .
EGF an d th e sugar s attac h to on e anothe r i n the intercellula r substanc e i n th e
walls o f blood vessels; whe n th e tissue s are injured, EG F an d the sugar s ar e released together . The presence in the blood of EGF attache d to sugars is a reliable
indicator tha t bloo d vessel s hav e indeed bee n injure d an d tha t ther e reall y is a
need fo r repair.
Like an y signals , chemical signal s between competin g organism s have to b e
reliableotherwise they will not be accepted by potential receivers . Chemical signals withi n th e multicellula r bod y als o deman d reliability : no t becaus e o f
conflicting interests , bu t rathe r t o preven t mistakes. 14 I f w e ar e right , the n al l
chemical signalsincludin g signal s withi n th e bodywor k accordin g t o th e
Handicap Principle . I t shoul d therefor e be possible t o find a logical relationshi p
between th e structur e of molecules used in signaling and the messages they carry.
This premise guides our current research into the messages encoded i n molecules
that ar e used in chemical communication.
P A R T I I
THE HANDICAP
PRINCIPLE I N SOCIA L
SYSTEMS
C H A P T E R 1
TESTING TH E BOND
t the end of each workday, when we arrived at home, our little daughters
used t o com e runnin g t o welcom e us . They would jum p up o n u s and
demand tha t we take part in their game s or a t least tell them a story, no
matter how exhausted we were. Our dog , too, would leap up and insistently push
himself agains t us . An d i n th e morning s th e do g woul d mak e eve n mor e o f a
nuisance of himself: he would li e down i n the doorway , forcing us either t o walk
around him or to push him aside every time we went from the kitchen to the dining
room.
All of us, including the dog , knew that we belonged together an d were willing
to d o a lot fo r eac h other. Bu t eve n in the mos t loving family, th e degree o f willingness an d abilit y to cooperat e ma y well chang e fro m da y to day . Thus, on e of
the mos t important question s fo r eac h membe r o f a partnership i s the degre e t o
which other partner s ar e willing to d o things fo r it at any given time. The eterna l
questions "D o you still love me?" and "How muc h do you love me?" are especially
urgent when on e o f the partner s ha s been awa y for a time, or i s getting read y to
leave. Our childre n and our dog revealed t o us the existence of behavioral systems
that enable individuals to collect information about the social bonds between the m
and their partners.1
111
TESTING B Y IMPOSITION
How ca n on e ge t reliabl e informatio n abou t th e qualit y an d strengt h o f a social
bond? Action s tha t benefi t anothe r ar e likel y t o b e accepte d b y hi m o r he r fo r
their own sake. The only way to obtain reliabl e information about another' s commitment is to impose o n that otherto behave in ways that are detrimental to him
or her . W e ar e al l willing to accep t another' s behavio r i f we benefit fro m it , bu t
only one trul y interested i n the partnershi p i s willing to accep t an imposition. As
we shal l see , al l mechanism s use d t o tes t th e socia l bon d involv e imposin g o n
partners.
People who don' t lik e dog s will no t le t a dog jump up o n the m o r lic k thei r
hands. Almos t anyon e would fin d i t too muc h o f an imposition t o be jumped o n
by a large dog like a pointer o r a German shepherd . Suc h dog s us e their weigh t
to test th e bond : the y approach an d stan d nex t t o a visitor in a friendly manner,
leaning agains t th e visitor' s legs , graduall y transferring more an d mor e o f thei r
weight, unti l the y ar e pushed off . How muc h o f this treatmen t a visitor will tak e
before pushing the dog off enables the animal to assess the visitor's attitude toward
it. When a dog gets in its owners' wa y in the morning, the way they move it aside
or g o around i t when the y are in a hurry gives it the informatio n it seeks. And a t
the en d o f the workday , a dog ca n fin d ou t reliabl y withi n a minute ho w muc h
attention it s owner s ar e willing t o giv e it jus t then , b y how willin g o r unwillin g
they are to be jumped up on.
Information abou t th e importanc e of a partnership t o eac h o f its members is
useful o n severa l levels . I n th e mos t extrem e cases , it ma y lead t o a decision t o
break u p th e partnership . Mos t o f th e time , though, i t help s individual s decid e
how much t o inves t i n a partnership an d ho w much ca n reasonably be expecte d
from th e othe r partner . Clearly , there i s no poin t i n asking for somethin g fro m a
partner wh o has no interest in the partnership .
But eve n amon g willing partners ther e ar e ofte n conflict s o f interest . A cake
eaten by one is not available to another. A moment of attention given to one partner
is a moment not devoted to a third. And even when all members of the partnershi p
benefit equall y from a n action, if one partner carrie s out th e actio n when anothe r
might have, it ca n be see n as a loss to th e on e and a gain to th e other .
The importanc e o f a partnership t o it s members an d th e relationship s amon g
partners depen d o n man y factors that ca n easil y change , which make s frequen t
testing o f the socia l bon d essential . It i s important t o eac h t o b e awar e o f other
partners' attitude s at any moment: it can be costl y to make a request a t the wrong
time, because onc e it has been denied , i t may be less likely it will ever be granted .
It is better t o asses s things first and wait until the odds ar e on one's side .
Testing th e Bond 11
AGGRESSION IN COURTSHIP
An individua l can test a social bond only by imposing upon another . The degre e
of impositio n depend s o n th e importanc e o f the informatio n sought an d o n th e
state of the bond. During earl y courtship, th e ris k involved in a decision t o mate
is very high, and the preexistin g investment i n the partnershi p small . Under such
conditions, th e impositions ten d to be high.
Some courting males behave aggressively toward females; most females respond
by leaving , an d th e mal e thu s find s ou t whic h one s ar e trul y interested i n him.
Such aggression is especially common among birds when both the male and female
invest a lot in their offspring. In many such species, males first establish territorie s
and the n wait for females to join them. The male attacks every female who shows
up i n his territory, and th e females fly away. Some of the females come back again
and again . Gradually, the male's aggression toward one of the females lessens and
then disappear s completel y o r almos t completel y fo r th e duratio n o f their lives
together. Israelis are familiar with pairs of wagtails, small European songbirds that
winter in Israel; the wagtails go through this process every fall, though they do not
breed together; they only cooperate in defending their feeding territory,2 and each
of them travels north alon e in spring to breed in Europe with a new partner.
As w e se e it , thi s hig h leve l o f aggressio n
early on is the simplest way for the male to test
the intentions of females who are proposing t o
share his property (his territory) and his future.
A female might find it convenient t o settl e in a
territory on a temporary basis , so as to hav e a
secure plac e t o ea t an d resid e while searchin g for a permanent mat e amon g the
neighboring males . Such a temporary arrangement would benefi t the femal e but
could harm the male considerably, because during that time other desirable females
who migh t otherwis e choos e hi m woul d no t approac h him . B y chasing a newly
arriving female , th e mal e test s he r intentions . A femal e who regard s hi m a s a
temporary convenience will not put up with being chased as much as a female who
has alread y decided that this territory and thi s male are her permanent choice .
In textbook s thi s aggression of males toward female s is explained a s resulting
from th e fac t tha t male s have to be highly aggressive in order to chase rival males
away from thei r territory; 3 they cannot ris k accepting females, whose appearanc e
is suspiciousl y simila r to tha t o f th e riva l males . I n tim e the y learn t o accep t a
particular female and sto p attacking her. This is no more than a description of the
facts presented a s an "explanation," and is an insult to the birds' perceptive ability.
Male babblers, too , chas e females who tr y to join their group . The y continu e t o
attack female s t o a lesse r exten t throughou t thei r lon g live s together ; bu t the y
hardly ever attack adult male members of their ow n group. 4 There i s no reason t o
suppose that a male is unable to differentiate between male s and females and limit
114 TH
its aggression to male s only. In fact , i n nonmonogamous species, where male-onmale aggression is especially high, there is very little aggression towar d females. 5
Testing th e Bond 11
Testing th e Bond 11
means by which babblers test the social bond amon g group members. The morning
dance takes place almost exclusively at the first light of day . It happens only once
every several days, and it is not yet clear what makes the babblers decide to dance
on a particular day. One of the babblers suddenl y stops at a suitable "dance floor "
and start s preenin g itsel f nervousl y o r sprawlin g wit h it s throa t touchin g th e
ground. Sometimes there is no response, an d the babbler give s up an d goes off to
look for food.
At other times, though, another babbler comes and clumps with the first, preening its own body. Two babblers clumpin g and preening ar e an almost irresistibl e
invitation, an d i n most case s th e res t of the grou p soo n join s in . The danc e ca n
last up to half an hour and sometimes even more. During the dance, babblers press
against eac h other , squeezin g under an d ove r an d betwee n thei r partners . The y
dance in the open, near a bush, even though the y could dance more safely under
trees.
The danc e almos t alway s take s plac e befor e sunrise , when th e dange r fro m
raptors i s greatest, since they can exploit th e low light an d surpris e th e babbler s
with relative ease. This is also the best time for babblers to feed, since many night
creatures are still activeincluding termites, a favorite babbler food. In short, the
dance doe s no t happe n a t th e easies t tim e and plac e but, o n th e contrary , at an
inconvenient tim e an d place , using inconvenien t movements . A n individual who
is willing t o undertake all this with it s partners shows reliabl y it s commitment t o
the group. The dancing of babblers reminde d us of stories our parents' generation
told about the dancing of members of pioneering kibbutzim in Israel in the earliest,
most difficul t an d exhaustin g years : "Fo r month s w e had nothing to eat, but we
danced al l night... ."9
Group ritual s that test the social bond ar e not unique to babblers. Other social
animals hold the m too , ofte n befor e other grou p activities . African huntin g dogs
jump on each other before embarking on a hunt.10 The hunt is risky to the hunter:
when it grabs the leg or neck of large prey and hang s on, its safety depends o n its
partners' cooperation . Africa n dwar f mongooses hold simila r rituals. 11 The nee d
to test the bond may even explain why dogs jump all over and around their owners
when settin g ou t o n their dail y walk. An d there are the dail y greeting s betwee n
humans. Kisses , handshakes, and th e exchang e of nod s an d verba l greeting s all
help us assess the attitud e of our partners, friends, associates , and coworkers during the openin g moments o f each encounter . I n chapte r 1 8 we shall se e how th e
sexual ac t became a means of testing the bon d betwee n partner s for various animals.
C H A P T E R 1
PARENTS AN D OFFSPRIN G
parent and a child are the simplest reproductive coalition there is. At first
glance, it seems obvious that both parent and child have the same interest:
the goo d o f the child . Bu t i f that i s so, why ar e ther e s o many conflicts
between parent s and children?
According to Trivers,1 the picture is less simple than it first appears. The child's
interest is to take care of itself, while the parent ha s to take care of other offsprin g
as well. The chil d aims to get from it s parent whatever it can get, even if the parent
shortchanges an d perhap s eve n lose s it s othe r offspring . Th e paren t want s th e
child t o succeed , but onl y if its investment i n that one chil d doe s no t reduc e th e
total number o f successful, reproducin g offsprin g i t can have.
A good exampl e of a mother-child conflict i s the nursin g and weaning of baby
mammals. Trivers explains the crie s of a baby who wants to nurse as a psychological weapon aime d a t making the mother nurs e it against her will. He assert s that
the baby does al l it ca n to forc e th e mother t o nurse it, while the mothe r trie s to
avoid nursing when nursing is against her ow n best interests.
Everybody know s tha t a screamin g bab y ca n forc e a mothe r t o action s sh e
would not otherwise take. But why exactly are mothers moved by a baby's screams?
Labeling th e scream s a "psychologica l weapon " doe s no t explai n what it i s that
119
12O
makes them effective. Trivers did not take into account that behavioral mechanisms
themselves evolve by natural selection.2 If mothers who did not respond to screaming, o r who did not respond a s much, had had more successful offspring than ones
who responded, then th e tendency not to respond woul d hav e spread in the population, an d the "psychologica l weapon " woul d hav e lost its potency. Behavioral
mechanisms are only proximate factors in the evolution of traits; the ultimate factor
in evolution i s successful reproduction .
Parents and
121
climbed t o the top o f a tree an d crie s all night long. Kindly neighbors tr y to hel p
it, assuming that i t has lost its mother. We think the kitten i s trying to blackmail
its mother into continuing to nurse it, to prevent the kitten fro m wanderin g off to
dangerous places . Th e dange r tha t th e kitte n wil l expos e itsel f t o predator s i s
greater tha n th e potentia l benefi t t o th e mothe r o f weaning it early. And a s long
as the benefi t of additional nourishment is greater than the ris k of predation, it is
in the offspring' s interes t t o cry.
Yet th e ris k involve d i n th e crying is , an d ha s t o be , realotherwis e th e
mother would no t submi t t o th e blackmail . S o from tim e to time , a fledgling o r
a kitten may be eaten. The young of hares and gazelles, who have many predators,
cannot affor d t o us e cryin g as a weapon; th e ris k is too great . They lie quietly in
a hidin g place , an d th e mothe r come s fro m tim e t o tim e t o nurs e them . Obvi ously, th e mothe r doe s no t nee d t o hea r he r babie s cryin g to fin d them . I f th e
young of hares and gazelle s have any way of blackmailing their mothers, we have
not foun d i t yet.
The ris k of predation i s not th e onl y factor tha t influence s parents . Even hu mans, who live far from predators , give in to their children' s cries . Of course , the
lack of predators and enemie s "allows" babies to cry as much as they care to with
no risk, which according to the Handicap Principle should greatly reduce the value
of cryin g as a signal . S o why d o parent s respond ? Protracte d cryin g by a baby
harms th e adult' s prestig e b y makin g a ba d impressio n o n hi s o r he r partner ,
neighbors, an d friends . Prestig e ha s rea l value, a s we shall see in a later chapter .
It may well be in the parent's interest t o give in rather than lose face .
124
C H A P T E R 1
BABBLERS, COMPETITIO N
FOR PRESTIGE , AN D TH E
EVOLUTION O F ALTRUIS M
viduals whose rank is higher than it s own, it may waver briefly, the n swallo w th e
food. Whe n th e bet a male , the number-tw o mal e of a group, goes up t o th e to p
of a tre e t o stan d a s sentinel , w e ofte n se e th e alph a male , hi s superior , busil y
looking fo r food; he then gives it to the sentine l in full vie w of the other member s
of the group and replaces hi m on guard duty. In many cases, we can tell when the
sentinel notice s th e alph a male' s preparation s t o fee d hi m fro m th e directio n of
the sentinel' s gaze , and ofte n becaus e the sentine l abandon s his lofty pos t befor e
the alph a male arrives to displac e him .
Our tea m check s on each group o f babblers i n the researc h area about onc e a
week, bu t ofte n mor e frequently. Thu s w e closely follow changes in the compo sition an d routin e activities o f each group . Over the year s we have learned their
life histories an d social structure. Detailed studie s have focused on specific aspects
of babble r behavior : sentine l activit y (Tirza Zahavi , Ton y Larkman , Nir Faran),
territoriality (Arno n Lotem), the feedin g of young (Thams i Carlisle) , allofeeding
among adult s (Ami r Kalishov) , playin g (th e late Ori t Pozis) , mobbin g (Zahav a
Carmeli, Avner Anava), allopreening (the late Andres Gutman), the morning dance
and feedin g a t th e nes t (Ron i Osztreiher), shout s (Zoha r Katsir) , wate r balanc e
(Avner Anava), and competition ove r mating (Yoel Perl).1 Kim Lundy and Patricia
Parker carried ou t DN A studies , Dietmar Tod t an d his students ar e studying vocalizations, and Jonathan Wrigh t i s studying feeding at the nest. 2
128 TH
and dangers, is not totall y hopeless. Occasionally , on e of them will live for months
or even years near its old territory, hiding from th e territory holders, until it finds
a grou p that accept s it a s a member o r manage s t o fin d a vacant are a an d join s
with other nonterritorial s to for m a new group.
Babblers ar e long-lived and ma y reach the ag e of twelve or fourteen. In years
of drought , when foo d is scarce, babblers d o not breed . I n rain y years, when th e
Arava Desert get s a few centimeters o f rain at the righ t intervals, a group of babblers ma y produce tw o or three successive broods. Becaus e of the combination of
breeding succes s and lon g life , man y individuals wh o canno t fin d a territory of
their ow n t o bree d i n g o on livin g wit h thei r parents ; thei r parents ' territorie s
provide enoug h food t o support the m all , and those parent s ar e still able t o raise
new offspring successfully. Tha t arrangement improve s th e lif e chances o f all parties. Parent-offspring group s are stronger than pairs without offspring; a s a result,
even i f an area becomes vacant , new settler s i n it have to for m group s i f they are
to protect themselve s against the families aroun d them. As a rule, new groups that
form includ e a t least three adult babblers .
13O
altruistic action. Trivers' s solution to the question o f altruism, then, begs the question, sinc e his enforcement mechanis m itsel f demand s altruism . Axelrod 15 ra n a
computer simulation that found that punishing individuals who do not reciprocate
will work, but onl y if any individuals who do not punis h are themselves punished
as well. Th e proble m i s that punishin g demand s effor t i n it s own right . Axelro d
concluded tha t th e mos t efficien t wa y to preserv e social norms is to have professional law enforcers suc h a s police, inspectors, an d judgeswho are paid to d o
the punishing. Of course , such professional enforcers do not exis t in nature.
Trivers's theory of reciprocal altruism was accepted
by th e scientifi c communit y as an important explanation of altruism between nonrelate d individuals. There
were two reasons for this: first, there was no other theory tha t explaine d th e man y case s i n whic h grou p
members clearly invest in the goo d o f the group, even
though the y have n o geneti c relationshi p t o on e another; an d second, Trivers's theory seemed to be supported b y the many instances in nature where altruism
was indeed reciprocated .
The theor y of reciprocal altruism led to the devel opment o f comple x mathematica l models , lik e th e "tit-for-tat " model. 16 Thes e
models investigate d through compute r simulation s under what condition s o f reciprocity altruis m would b e desirable . Wit h al l their sophistication , none o f these
models manage d to resolve the greatest problem pose d by the theory of reciprocal
altruism: How ca n one who does a favor fo r another ensure that the favo r wil l be
returned?17
Sentinel Activities
Let's take th e babblers ' sentine l activitie s as an example. When babbler s fee d i n
the morning, on e of the group often perches on a tall branch o r a treetop. Whe n
this sentine l see s danger , i t issue s "alar m calls" 19which, a s we hav e said , ar e
directed a t th e approachin g predator , bu t whic h als o aler t th e group . Standin g
guard means exposing oneself to danger and forgoing food until the watch is over.
Individual babblers may spend up to two or three hours a day standing guard. All
group member s tak e part , a fac t whic h a t firs t seem s t o suppor t th e theor y of
reciprocal altruism. But more detailed observation shows that the babblers ar e not
at al l interested in having others do a fair sharetha t is, in reciprocity .
Tirza Zahavi 20 foun d tha t higher-rankin g babbler s stan d guar d mor e tha n
lower-ranking ones do, and that they interfere in the guardin g done by their sub ordinates; the y often expe l their subordinate s fro m th e guar d post an d tak e thei r
place. When a lower-ranking guar d refuses to leave its post, a higher-ranking bab bler wh o come s t o replac e i t may shove it an d eve n hit it . On th e othe r hand , a
babbler tryin g to replace a guard higher in rank than itself does s o by sitting on a
lower branchsometimes on a lower branch in another treean d waiting for the
guard to leave; only then does the lower-ranked replacement go up to the dominant
babbler's pos t (se e Graph 12-1) .
As a rule, the guard clearly sees the one attempting to replace it: one can observe
it preening its feathers, shifting around, at times climbing to an even higher branch.
The sentinel is certainly in no hurry to take advantage of the other's offe r an d leave
Graph 12-1. A typical sequence of sentinel activity in the morning in one group; a
downward arrow shows replacement. The dominant male (Ml) and the dominant
female (Fl) both stood guard first thing in the morning. The third male (M3) came up
to replace the dominant female only after Ml went down; he was several times
replaced by the beta male, M2, and once by the alpha male, Ml. M2 in his turn was
repeatedly replaced by Ml. When the second female (F2) tried standing as a sentinel
on another tree, she was immediately replaced by the top female (Fl). Throughout this
time, a young female (F3) stood guard intermittently; none of the others bothered to
replace her.
its post. A romantic view would sugges t that dominant babblers ar e volunteering
to serve in the place of tired comrades who are younger and less experienced, bu t
detailed observatio n show s tha t thi s is not th e cas e a t all . Eac h make s th e mos t
effort t o replac e the on e just belo w i t in rank, who i s likely to b e closes t to i t in
age; individuals ar e considerably les s likely to replace much younger group members.
If guardin g were based o n reciprocity, there would b e n o point i n striving to
do more guard dut y tha n others . Eve n i f on e assert s that suc h competitio n i s
necessary t o ensur e tha t th e grou p i s neve r withou t a sentinel , on e woul d stil l
have t o explai n wh y each bir d interrupt s th e watc h o f the on e neares t t o i t i n
rank, rathe r tha n attemptin g t o replac e younger , more inexperience d babblers .
The dominan t male' s interferenc e wit h th e guardin g don e b y th e on e nex t t o
him i n ran k ca n become s o intense that that second-ranke d bird, th e bet a male,
ends u p guardin g much less than th e thir d i n rank , with who m th e top-ranking
bird interfere s less (se e Graph 12-2) .
This does not happen because of any lack of desire to guard on the part of the
beta male : in fact, th e beta male goes up to guard more frequentl y tha n th e third
in rank ; th e reaso n h e end s u p guardin g les s i s tha t th e alph a mal e keep s in terrupting hi s guar d duty . I t s o happened tha t i n tw o o f th e group s i n whic h
detailed studie s of guarding were done , th e dominan t males disappeared durin g
the study . In bot h cases , once the dominan t disappeared , the one next to him in
136
Graph 12-2. Number of shifts and duration of watch of males Ml, M2, and M3 in one
group. M2 came up to stand guard more often than M3 (M2 took more shifts), but his
total sentinel activity was less, because the alpha male replaced him frequently.
Graph 12-3. Duration of watch for males M2 andM3 in several groups, relative to the
duration of watch for the alpha male (Ml); note the reversals in groups G and H after
their alpha males disappeared (G' and H'). Ml = 100%. Maximum duration: 2.5
hours/day in group H. Minimum duration: 0.5 hour/day in group C.
ranknow the top maleimmediatel y started guarding much more tha n before
the chang e (se e Graph 12-3 , groups G' an d H') . Befor e the dominan t mal e disappeared, th e bet a male s in these groups ha d bee n guardin g less tha n th e third ranked males ; after th e change , when th e dominan t wh o represse d th e bet a was
gone, th e sam e birds wer e guardin g far more than th e formerl y third-ranke d individuals (se e Graph 12-3) .
Feeding of Nestlings
Babblers als o compet e ove r the feedin g of nestlings.
Thamsi Carlisle 21 foun d tha t higher-rankin g one year-old babbler s actuall y interfere with othe r bab blers o f th e sam e ag e when thos e bird s tr y t o tak e
care of the group' s young . This ca n reach surprising
extremes: Carlisl e observe d case s in which a group
of a dozen babbler s ha d onl y one surviving nestling,
and four or five babblers would come to the nest with
food i n thei r beak s a t th e sam e time. Eac h ha d t o
waitwith food in its beakuntil all those that outranked it had finished feeding
the sole nestling. Sometimes the lower-ranked birds would not even dare approach
the nes t (se e Graph 12-4) . If th e onl y function o f feeding nestlings is to nurtur e
the nestlings , why on eart h d o babbler s preven t other babbler s fro m doin g jus t
that?
138
Graph 12-4. Visits to nests by yearling helpers, as percentage of mean visits. Data and
graphs by Thamsi Carlisle (Carlisle and Zahavi, 1986).
Left: Visits to unattended nests. Summary of 598 visits to 4 nests by 3-9 yearling
helpers. When there was no other bird at the nest, there was no apparent relationship
between the rate of visits to the nest and the helper's rank.
Right: Visits to nests where the incoming helper had to replace another at the nest.
Summary of 187 visits to 3 nests by 3-9 yearling helpers. The solid line indicates that
the lower the rank of the incoming bird, the less frequently it came to the nest when
another helper was there.
other frequently. The y may even switch ranks during their first year of life. Thamsi
Carlisle23 recorde d 9 4 cases of fledglings and yearling s feeding each other . I n 8 6
cases a yearlin g offere d foo d t o it s subordinate . I n 2 5 o f thosewel l ove r a
quarterthe subordinate refused th e offere d foo d or only tasted it. In 7 of these
25 case s of refusal , th e would-b e feede r chase d th e subordinat e an d sometime s
pecked at it. Only in 8 cases did a subordinate yearling offe r foo d to one rankin g
above it. In full y 6 out o f these 8 instances, the dominan t yearlin g refused to eat
and attacke d the would-be feeder. In Carlisle' s research , most feeding was don e
with breadcrumbs given to the birds by the observer. More recently, Amir Kalishov
studied allofeedin g amon g adul t babbler s withou t offerin g the m any food ; his
findings were similar to Carlisle's. 24
In one case in Carlisle's study, an eight-month-old female tried to feed her tenmonth-old sister; the latter stood up , snatched the food out of her younger sister's
beak, forced he r t o crouc h lik e on e begging fo r food, an d then stuffe d the foo d
down he r throat . Onc e th e younge r bird ha d swallowe d th e food , the dominan t
sister pecke d he r unti l sh e fled. The frustrate d younger sister then too k anothe r
crumb and went to feed her subordinate younge r brother, who was hunting quietl y
for foo d some thirty feet away.
In anothe r caseone of the tw o instances in Carlisle's stud y in which the gif t
of food was accepted b y one higher in rank than the feederthe dominant fledg-
139
ling accepted th e foo d but the n attacke d th e feeder and kicked i t in the face, a s if
to say "I'll tak e this food, bu t I still outrank you." Fa r from rewardin g altruistic
behavior an d returnin g ti t fo r tat , babblers who ar e offered foo d b y their subor dinates actually punis h them fo r making the offer. I f the function o f feeding other s
were to benefit the ones being fed, why would th e recipients o f the benefit punis h
their benefactors ? Babbler s behave as though i t is the ac t o f giving, rathe r tha n
the benefit given , that matters .
Mobbing
Babblers' mobbing is generally simila r to that of other vertebrates. A babbler who
notices a snake or a raptor will sound a tzwick and then make barking an d trilling
sounds. This alerts th e other members of the
group, wh o arriv e an d approac h th e raptor .
When a babbler comes within four to six feet
of th e raptor , i t spread s it s tai l an d lift s it s
wings, fannin g the m out . I t holds that stanc e
for severa l seconds; it may turn sideway s and
circle the raptor , tai l an d wing s stil l spread .
These display s last a minute o r two , an d th e
babblers' movements chang e accordin g to the
degree of danger. Zahava Carmeli, who studied babblers' mobbing of snakes, found tha t the babblers were well aware of the
risk: she determine d tha t o n averag e mobbing babbler s kep t a distance o f 1 0 to
15 inches from a snake's tail , but the y kept some 20 inches from its head, whic h
would indicat e tha t th e bird s kne w ful l wel l whic h en d o f th e snak e pose d a
danger.25 If the babblers attacked the snake at all, they aimed at its head. Mobbers'
behavior varie s a great deal : som e div e headlon g int o danger , other s hol d back .
Different babbler s stop at different distance s from th e predator.
The tendency o f a babbler to mob correlate s to the social makeup of its group.
Avner Anav a studied babblers ' mobbin g o f raptors , ofte n usin g stuffe d models .
Two of the groups he studied comprise d one adult male living with several females
and year-ol d fledglings; in thes e groups , th e dominan t mal e di d no t participat e
much i n mobbin g (se e Grap h 12-5 , grou p HAK) . I n group s wit h severa l adul t
male members, all those adul t males participated muc h more. In these groups, the
dominant mal e alway s mobbe d longe r tha n th e other males , cam e close r t o th e
raptor, stoo d guar d during mobbin g mor e than others , and actively disrupted th e
mobbing activitie s o f th e other adul t male s (se e Graph s 12- 5 an d 12-6 , group s
ZEH an d MZR).
The activitie s o f the second - an d third-ranking males depended mostl y on the
relationships betwee n the m and the first male. When such males accepted unquestioningly the position of the dominant malefo r example , if they hardly made any
Graphs 12-5 and 12-6. Competition over mobbing and interference with mobbing. Data
from Anava, 1992. At the time, group MZR comprised a father (Ml), a mother (Fl),
an adult son of the father but not of the mother (M2), and a son and a daughter of
both father and mother (M3 and F2). Group ZEH comprised three sibling males and a
female who was not related to any of them. Ml and M2 were from the same brood,
and during the course of the study there was intense conflict between them; eventually,
Ml disappeared probably ousted by M2, who then took his place. Group HAK was
composed at the time of a father (Ml), a mother (Fl), their daughter (F2), and a
stranger female who had recently joined the group (F3).
Graph 12-5 (top): Position relative to the raptor: nearest = 1, farthest away = 4. In
the MZR and ZEH groups, the dominant males were almost always the ones nearest
the raptor, and the dominant females, who were the only adult females in each group,
stayed farthest from the raptor. In group HAK, which comprised one adult male and
three adult females, the dominant male stayed farthest from the raptor, and the
dominant female came nearest.
Graph 12-6 (bottom): Interference during mobbingwho interferes with whom.
In the MZR group, no one interfered with the dominant male (Ml). The dominant male
himself interfered a great deal in the mobbing activity ofM2. N o one interfered with M3,
but M2 interfered with the dominant female (Fl), and M3 interfered with his sister, F2.
In the ZEH group, Ml interfered a great deal with M2, but M2 also interfered with Ml. Both
Ml andM2 interfered with M3Ml more than Ml. M3 interfered with the female only.
In the HAK group, Ml did not interfere with Fl but did interfere somewhat with the
stranger female, F3. None of the other females interfered with Fl. Both Fl andF3
interfered with F2, and both Fl and F2 interfered a great deal with mobbing by F3.
142
Evidently, each babbler care s mainly about providing the benefit, rather than about
the actua l benefit s th e grou p receives . I f w e wan t t o understan d th e babblers '
altruistic behavior , the n w e hav e to determin e wha t th e giverth e "altruist"
gains from th e ac t of giving, rather than what th e grou p a s a whole gains .
It i s important to remember that grou p members of the same gender compet e
with eac h othe r ove r th e utmos t biologica l needth e chanc e t o reproduce . I n
spite of this rivalry, they hardly ever fight one another. In the vast majority of cases,
conflicts within th e grou p are settled by means of the competitio n ove r altruism.
How ca n altruism replace physica l aggression? This brings us back to the substitution o f threat s fo r actua l fightin g (se e chapter 3 , o n rivals) . Because o f th e
danger an d cos t inheren t i n fighting , t o bot h lose r an d winner , other way s o f
resolving conflicts evolved. Actual, all-out physical struggle was replaced by threats
that showe d wit h a reasonable degre e o f reliability how likely the threatene r wa s
to win an actual fight.
But threats have their own price. When threat s are not effective, the threatene r
does have to fightor forfeit. Th e stakes are highest when an animal issues a threat
in th e presenc e o f witnesses; when a n individual's threat s go unheeded, th e individual ma y fai l t o dete r no t onl y th e riva l bu t th e witnesse s a s well. Thus , th e
presence o f witnesses tends to make threateners less likely to compromise. More over, witnesses who see a contestant injure d or spot som e weakness in one or th e
other may seize the opportunity and take over. This is especially true among highly
social animals like babblers, wh o ar e always together. An y threat not followe d u p
by action , an y unsettled conflict , an y failure of a dominant membe r i s noticed b y
the entire groupcomrades who are also potential rivals .
Yet conflict s d o occur an d deman d resolutions o a substitut e for threaten ingwhich itself evolved a s a substitute fo r fightingi s highly desirable. Actions
that ar e not direc t threat s but ar e closely relate d t o a n individual's abilit y to win
a struggle can take the plac e o f threats. By showing off how much they can invest
in standing guard, in feeding their comrades, in taking risks, and in other altruistic
acts, babblers show off their ability to win in a fight and their desirability as groupmates. The altruist's investment in the altruistic ac t offer s a reliable , concret e inde x of
that individual's ability.
Altruistic acts have another benefit : they
prove th e giver' s interes t i n th e receiver ,
even whil e the y proclaim th e giver' s domi nance. By investing in the good of the group,
the dominan t mal e show s of f both hi s su periority an d hi s willingnes s t o giv e t o hi s
subordinates. Thi s make s thes e subordi nates les s likely to leave and thu s helps th e
dominant bir d remain at the head of a large,
strong group.
Other grou p member s hav e good reaso n t o pay attention whe n an individual
acts for the group's benefit: what they learn about that individual helps them avoid
a high-ris k fight against a rival stronger than the y are. All members of the grou p
must constantl y be assessin g thei r prospects . Afte r all , eac h bir d ha s t o decid e
whether to sta y on in the grou p as a subordinate, leave and tr y its luck elsewhere,
or ris k everythin g in a fight for th e to p position . Altruisti c acts that benefi t th e
group help each babbler answer these very questions.
144
well-being of others, prestige can be won by unprovoked aggression , whether physical attack or threat. Such aggression is so common that social ranking is also called
"pecking order." 28 Prestige ca n als o b e acquire d b y "wasteful " showin g off ; the
peacock's tail, the deer's antlers, an d the bowers built by bowerbirds are examples
of showin g of f tha t i s neither harmfu l no r usefu l t o others . Babbler s an d othe r
altruistic animal s gain prestig e b y investing in thei r fello w grou p members ' well being. Their partner s benefit, bu t th e reaso n for their altruis m lies elsewherein
the real testimony to their abilit y that it provides .
Social rank is easy to discern; prestige, o n the other hand, is complex and harder
to measur e precisely. Prestige reflect s th e degree o f a superior individual' s dominance, as recognized by subordinate members of the group. In othe r words, prestige is gauged by others. The dominan t ma y claim prestige, but fo r the prestige to
be real it has to be accepted by subordinates, and it is this acceptance that actually
determines a n individual's prestige .
Prestige ha s real value: a dominant male with higher prestige ca n get with ease
what a dominant mal e with les s prestig e gets only with grea t effort , o r no t a t all.
Babblers mak e constant , unceasin g effort s t o stres s thei r ability , no t t o ris e i n
rankan adult babbler ca n only "promote" itself by killing its superior or chasing
it from th e group, o r by leaving the group itselfbut t o persuade their comrade s
to recognize tha t abilit y and grant them prestige . A babbler who ca n stand guard
longer tha n it s comrades , giv e them par t o f its food, approac h a raptor, tak e th e
risk of sleeping at the exposed end of the rowand can also prevent others from
doing such deedsproves daily to its comrades its superiority over them. By doing
so, that individual increases its prestige an d ha s an easier time exerting control .
Greater prestige means that subordinates will avoid getting into a fight for the
higher position . Greate r prestig e convince s the female to stay faithful t o the dominant mal e an d not t o mate wit h hi s subordinates. In short , a babbler's altruistic
acts ar e a n investmen t i n it s prestige , an d tha t prestig e ha s real , concret e value .
The difficultyth e cost , or handicapof this altruistic advertising, whether foo d
sacrificed o r danger incurred, i s what makes it a reliable indicator o f the abilit y of
the advertiser .
Subordinates hav e their ow n prestige, whic h is shown by their abilit y to resis t
their dominants and by their superiority over those below them. Babblers replace d
during guar d dut y o r fe d b y on e mor e dominan t tha n the y ofte n tr y t o regai n
prestige a s bes t the y ca n b y replacin g a lower ranking guard, or by attacking a bird of a differen t
species, lik e a bulbu l o r a blackstart . Th e fre quency of these behaviors shows clearly both that
individual babbler s ar e ver y awar e o f thei r ow n
prestige an d tha t man y of their actions , especiall y altruistic actions , ar e done to
gain prestige .
We als o find abundant evidenc e that othe r grou p member s ar e well awar e of
their comrades ' claim s to prestige. Subordinat e male s often approac h a female or
a lower-ranked male who is standing guard, feed it , and take its place as a sentinel;
in som e groups, this almost alway s provokes a reaction fro m th e dominan t male,
who hurries to feed the subordinat e guar d and replace him. Sometimes the dominant male stands guard only for a moment before leaving the guardpostas if to
say that hi s only intention wa s to make his rival stand dow n an d asser t his superiority, which may have suffered slightl y from the subordinate's displa y of prestige.
146 T H
intense within day s of her arriva l in the group. At that point, the new female doe s
not yet know the group well; moreover, the senior subordinate males in the group
are not he r offspring , an d thu s al l of them ar e eligible t o copulat e with her . Th e
new female can learn the males' ranks quickly and easily, but ran k alone does not
tell her th e degre e o f control th e dominan t mal e has over his subordinates. Ho w
much doe s h e need them ? How much do they recognize his dominance?
The new female has to split her male suitors' chance to breed according to the
balance o f powe r amon g them , bu t ho w ca n sh e fin d ou t wha t tha t balanc e of
power is if they live together in peace, with no overt aggression whatsoever? If the
female make s a n erro r i n grantin g o r withholdin g he r consent , sh e ca n en d u p
with a powerful, dissatisfie d male groupmate who wil l break he r eggs . We hav e
observed several cases of males breaking eggs in the nest under such circumstances.
The mai n victim i s the female , wh o invest s more i n producing egg s than d o he r
consorts.
The "shyness " tha t prevent s th e femal e fro m copulatin g i n th e presenc e o f
other babbler s help s he r determin e th e prestig e o f eac h maleor , t o b e mor e
precise, it allows her to see how much prestige each male is accorded by the others.
This enable s he r t o shar e he r favor s accordin g to th e relativ e importanc e o f her
partners. Th e dominan t male's prestige is demonstrated whe n other males refrai n
from followin g him an d the femal e eve n at a distance. Babblers who let the dom inant mal e retir e wit h th e femal e withou t eve n tryin g t o observ e the m fro m a
distance show their acceptance o f the dominan t male' s superio r prestige. By contrast, a male who follows with impunity displays to the female his own high prestige
as a subordinate .
A few days before egg-laying, the dominant male starts "guarding" the female. 30
He follow s the breeding femal e closely and keeps her in sight; at whatever time of
day, h e i s neare r t o he r tha n i s an y other grou p member . Whe n anothe r mal e
approaches her , th e dominan t mal e doe s s o too . I n mos t case s hi s approac h i s
enough t o caus e the subordinat e t o mak e the submissiv e sound o r show his discomfort b y fluffin g hi s feathers and preenin g himself.
The dominan t mal e alway s copulates wit h th e femal e more tha n an y o f th e
other males do. But other males, too, may copulate with the femal e if they are not
her offsprin g an d if she cooperates. I f the female wishes to copulat e with anothe r
male, she can always find the one or two minutes needed when the dominant male
is absorbed i n something else , such as a border conflic t or nest-building. I n som e
groups, subordinate male s manage to copulate with the female even on her fertil e
days an d eve n i n the mornings , which see m t o b e th e bes t tim e fo r fertilization.
Yoel Perl found that i n some cases the dominan t stops guardin g the femal e eve n
while she is still fertile, befor e the ovulation of the fourt h egg ; the secon d i n rank
then copulates with her and presumably fertilizes that egg.31 In other groups, males
of similar rank do not copulat e a t all. An individual's reproductiv e chances , then,
cannot be predicted by rank alone.
When the dominan t male allows his subordinates t o mate with the female , he
does so because he needs them in the group an d must therefore make concession s
to them. We think that th e position o f each grou p membe r depend s both on the
balance o f power withi n th e grou p an d o n th e group' s neighbors . Som e groups
have stron g neighbor s an d nee d mor e an d bette r fighter s fo r protection , whil e
others hav e weak neighbors . Som e dominan t male s ar e strong an d d o no t nee d
much assistanc e in fighting; others depen d more on their subordinates .
Another factor tha t ca n affec t th e balanc e of power withi n a group is that th e
more partners the dominan t mal e has, the les s dependent h e is on any single one
of them. And a dominant male with adult sons by the curren t dominant female
who do not mate with their motherdepends less on the assistance of other males
who might compete with him over copulation. Al l these factors affect cooperatio n
among males. Every group of babblers has one male who outranks all the others,
but som e dominant males let their comrades copulate, while others threaten them
or eve n pec k a t the m whe n the y try . Clearly , rank i s onl y par t o f th e picture ;
prestige, too, is a crucial element.
148 T H
its experienced comrades , rather than experimenting and possibly failing. Babblers
indeed benefi t fro m a n extende d perio d o f learning, durin g whic h the y acquire
both group-living skills and abilities that enable them to find food, avoid predators,
and dea l with strange babblers. Likewise , in a group setting, it pays to be inclined
to compromis e rather than quic k to fight over one's rights; we have seen that it is
exactly this temperament that characterize s babblers .
Adaptations such as these may compensate fo r the disadvantage s of group life ;
this may explain why the score s of species o f babblers in the Indian subcontinen t
all live i n groups , althoug h the y live i n man y differen t habitats , which ar e als o
occupied successfull y by solitary songbirds.32 After all , some adaptations are likely
to b e irreversible , sinc e the y involv e a comple x se t o f interconnecte d changes .
Reptiles an d mammal s wh o lef t th e lan d an d returne d t o th e wate r continu e
breathing through thei r lungs , even thoug h i n their ne w habitat i t would benefi t
them to breathe through gills. If babblers could all at once regain the characteristics
they los t i n adaptin g t o grou p life , the y migh t d o bette r a s pairs i n som e ne w
environments; as it is, they do better living in groups .
Some species of birds live in groups or in pairs
depending o n conditions . Seychelle s warblers ,
which usuall y live in groups , were transferre d i n
one cas e t o a n islan d withou t warblers . The y
formed pairs, nested, and increased in number until all suitable territories were occupied, an d then
they went bac k t o grou p living. 33 Fo r thes e warblers, grou p livin g seem s t o b e a relativel y new
development: unlike the babblers, they don't seem
to have group-living relatives.
Group livin g has develope d i n differen t spe cies for different reasons , and there are many different kinds of collaboration. Some
provide a n edge i n the competitio n fo r resources , whethe r wit h othe r specie s o r
with othe r group s o f th e sam e species . Other s affor d bette r protectio n agains t
predators o r adverse environmental factors. Among some birds, like the scrub jays
of Arizona , coalitions ar e limited t o parent s and adul t offspring ; i n suc h specie s
the adult offsprin g d o not shar e in reproduction. 34
Some other jays , som e Africa n starlings , an d long-tai l tit s for m coalition s t o
protect thei r territory . Each grou p i s made up o f several pairs, bu t eac h pai r has
its own nest. Individuals whose nest fails or who do not find a mate assist the other
pairs at their nest s and help protect th e commo n territory, but the y do not themselves reproduce. Th e groove-bille d ani s of Central Americ a for m ne w coalition s
every year, with several pairs sharing a single nest.35 Simpler coalitions may consist
of severa l female s wh o la y egg s i n th e nes t o f a singl e male , a s i n th e cas e o f
ostriches, o r o f severa l male s wh o hel p a singl e femal e rais e he r young , a s d o
Galapagos hawk s and the harrier s of Scotland. 36
ISO TH
C H A P T E R 1
152 TH
superior foodlik e th e honeybee' s roya l jelly. The caregiver s thu s divid e thei r
resources unequall y and depriv e som e of the offsprin g in a way that lessen s th e
latter's chance s to reproduce . Parent s exploi t som e o f their offsprin g b y making
them int o helpers who will assist them o r their other offsprin g t o reproduce .
The theor y of "parental manipulation, " a s it was
called by Alexander,2 assumes that the parent is concerned wit h th e su m tota l o f it s reproductiv e suc cessbut no t necessaril y wit h th e fat e o f on e o r
another offspring. 3 Thi s explain s th e benefi t t o th e
parent in exploiting som e of its offspring, but i t does
not explai n the other sid e of the question: Why does
the shortchange d offsprin g hel p it s parent? Alexander assume d that the theories of kin selection an d of
reciprocal altruis m explai n adequatel y why the represse d worker s assis t thei r re producing kin . We disagree.
154
and th e winne r kill s o r expel s he r partner s o r enslave s them. I n mos t case s the
colony ends up with one queen only, who goes on laying eggs, while her daughters
and the daughters of her former partners take care of the offspring. These workers,
who ar e not fertilized , cannot compet e wit h th e quee n effectivel y sinc e they are
smaller, an d sinc e she is the onl y one wh o ca n lay fertilized eggs to creat e more
workers.
In th e temperat e region s ther e ar e man y specie s o f hymenopter a tha t for m
annual colonies i n the spring, which di e out with the onse t of winter. This means
that i n th e sprin g there ar e no larg e colonies, an d a single queen ca n establish a
new nest on her own. For example, young queens of the wasp Vespa orientalis and
its relativ e Vespula germanicd 1 hatc h i n the fal l an d liv e for a while i n thei r birth
colony. A t tha t time , the y d o nothin g bu t ea t an d rest . Later , when th e colon y
nears the end of its life, each queen goes on a mating flight, then passes the winter
in hibernatio n i n a crack in th e soil , ofte n wit h siblings . I n sprin g sh e wakes u p
and start s building a nest, laying eggs, and gatherin g food for her offspring .
The firs t offsprin g o f such queens ar e females. They cannot mate , since there
are n o male s a t tha t tim e o f th e year ; s o the y function a s workers, helpin g th e
queen t o rais e additional offsprin g throughou t th e summer . Late in the summer
things change . Th e quee n start s layin g unfertilized eggsmal e eggsan d th e
workers star t giving some o f the queen' s fertilized eggs large quantities o f superior food ; thes e egg s develo p int o th e nex t year' s queens . A t th e sam e time ,
some of the mos t dominan t worker s manage to la y eggs: each take s over several
cells, whic h sh e protects , an d i n whic h sh e lay s unfertilize d (male ) eggs . Thus,
some of the male s tha t hatc h i n the colon y ar e offspring o f the workers, not th e
queen. The laying workers ar e very aggressive toward each other and toward th e
queen. The y ea t egg s laid b y their rival s and b y the quee n an d destro y the cell s
of thei r rivals.
Why d o thes e worker s sta y in th e colony ? Fo r tw o reasons . First, a worker,
being small , has no prospects o n her own against the other colonie s around, each
with a large queen an d a number of workers. The workers are small because their
mother ha s raise d the m t o b e small , and th e first workers ar e particularly small
because their mother has raised the m on her own and had a hard tim e bringing
in enoug h foo d fo r he r larvae . Second, a worker canno t la y female egg s to raise
daughter workers who would help her protect and take care of her nest. Thus, the
only way a worker that hatches in the spring can have viable offspring i s to survive
in a n establishe d colon y until th e fallth e tim e fo r raisin g queens an d males
and then attemp t to lay male eggs. Since she has to sta y in a colony, she may well
choose to stay in the colony she is familiar with and hope conditions will allow her
to bring up successful sons when the time comes. But she does have the option of
moving t o anothe r colony , an d i n fact , man y workers d o mov e fro m colon y t o
colony,8 presumabl y seeking a place where the y will hav e a better chanc e to re produce.
Discussions about colonies usually center on conflicts of interest between work-
156
ers an d queen , but i n fac t eac h worke r ha s her ow n individua l interests ; a large
part o f th e lif e o f a colon y make s n o sens e unles s conflict s o f interes t amon g
individual workers ar e taken int o account. 9 There i s an order of rank amon g the
workers. If the top worker were to kill the queen an d take her place, that worker
might b e abl e to lay her ow n unfertilized male eggs freely, bu t th e othe r worker s
would b e represse d b y that upstar t worker . An d thei r colon y would b e weaker;
only th e fertilize d quee n ca n strengthe n th e colon y b y layin g female egg s an d
creating more workers.
Each worker' s chanc e t o hav e sons, an d thos e sons ' chances , depend o n th e
well-being o f the colony , an d th e colon y ca n be strengthene d onl y by the queen .
So it is better fo r most workers to hav e a queen a t the hea d of the colon y than to
have another worker in that position. Each worker's chanc e to reproduce successfully conflict s mor e with that of the other workers than with that of the queen. T o
get th e bes t sho t a t havin g successful son s later, then , younge r worker s hav e t o
cooperate with the queen and suppress egg-laying by the highest-ranking workers.
No wonde r tha t al l summer long the colon y grows by raising more workers: the
workers themselve s preven t th e raisin g of princesses (youn g queens ) an d males ,
and they suppress an d kill workers who tr y to lay eggs.
In th e fall , th e cas e is different: th e colon y is nearing the en d o f its life . Th e
time is ripe to rais e new queen s an d males . The quee n begin s layin g unfertilized
male egg s a s well a s fertilized female eggs, and th e worker s star t givin g some of
the queen' s fertilize d egg s the treatment tha t will make them into futur e queens .
At thi s seaso n a struggle often break s ou t ove r the layin g of male eggs, both between workers and queen and among the workers. The winners among the workers
manage to lay some of the colony's male eggssometimes even most of them. The
workers who d o not manag e to lay male eggs help the quee n an d their egg-laying
comrades raise their young.
A simila r logi c applie s whe n existin g colonie s brea k u p int o ne w ones . T o
withstand neighborin g colonies, a colony o f wasps has t o avoi d breakups, whic h
would sprea d it s strength to o thin . In tha t situation , it is in the interes t o f workers t o suppres s th e raisin g o f princesse s an d th e layin g of mal e egg s b y othe r
workerssince, when grown , these would swar m and spli t th e colony . But onc e
the colon y is large enough t o becom e tw o viable ones, a split is in the interes t of
both quee n an d workers : th e quee n ensure s tha t a t leas t on e o f her daughter s
will have a colony o f her own , an d a t the sam e time, each worker's reproductiv e
chances increase , because sh e ha s hal f a s man y othe r indi viduals to compet e with .
Why can' t a worker strik e ou t o n he r own , buil d a few
cells, store food, and wait for the appropriate tim e to lay male
eggs? Becaus e hyme n op tera gathe r foo d fo r thei r offspring ,
such smal l nest s would b e destroye d b y members o f neighboring colonies , wh o would stea l anythin g stored in them to
feed thei r ow n larvae. This dange r create s the nee d t o coop -
erate in guarding and the opportunity for the strong to exploit th e weak. Robbery
and predation preven t th e workers from reproducin g outside large colonies ruled
by queens .
158
demonstrate and asses s their own and eac h other's abilit y without a physical clash
or direc t threats , and anything that will help them evaluat e a partner's interest in
continued collaboration , wil l increase their chances of success.
Thus ther e is a ready audience fo r messages that reliably combine evidenc e of
an individual's abilityas show n by its doing deed s that demand abilityan d of
its interest i n continued collaborationa s demonstrated b y its willingness to devote thes e show-of f effort s t o it s collaborators . B y helping, th e signale r demonstrates its ability, which is recognized by others; this recognition translates into the
rank an d prestig e tha t enabl e i t t o reproduc e mor e successfull y tha n individuals
who receiv e less recognition. This ca n become a powerful selective force fo r be havior that helps the group; the evolution of what looks at first glance like straightforward altruisti c behavior is in fact drive n purely by the mechanism of individual
signal selection .
1 6O TH
Roseler an d Hon k sho w that in bumblebee nests , the ovarie s of the stronges t
workers, who are nearest to the queen, are well developed eve n though their proximity to the queen exposes them to high levels of queen pheromone. Th e researchers remar k tha t thes e worker s d o no t hol d thei r hig h ran k because o f thei r
well-developed ovaries ; the worker s maintai n their ran k eve n if their ovarie s are
removed surgically . We thin k tha t thes e worker s ar e physically superior t o thei r
colleagues, and that this superiority gives them both their high rank and the ability
to develo p thei r ovarie s in spit e o f the hig h concentratio n o f quee n pheromon e
they are exposed to. 18
In honeybees, the queen pheromone contain s unsaturated fatty acids with keto
groups. I t i s known tha t fatt y acids , especiall y unsaturate d fatt y acid s with ket o
and alcoho l groups, are active, harmful chemicals . They are similar in structure to
the femal e mot h pheromone s w e hav e alread y discussed. I t ma y be tha t quee n
pheromone i s absorbed b y th e bee' s expose d sensor y cells an d cause s a state of
intoxication, a s we suggested for moths i n chapte r 9 . If we assume that a worker
who carrie s quee n pheromon e i s harme d b y i t i n thi s o r other ways , the n th e
amount a worker ca n carry is limited not onl y by her abilit y to acquir e it by forc e
or in exchange for services, and her abilit y to protect it , but als o by her abilit y to
withstand tha t harm.
Showing off by consuming harmful chemical s like alcohol, tobacco, betel nut,
opium, and the like is common among humans. In some societies, men even demonstrate their vigor by drinking naphtha. In his book The Rise and Fall of the Third
Chimpanzee, Diamon d uses the Handicap Principle to explain this phenomenon.19
Veblen,20 the sociologist who coined th e phrase "conspicuous consumption," lik ened the men who hang out in bars and pubs, drinking and buying drinks for each
other, to American millionaires wh o sho w off by funding colleges , hospitals, and
museums. On e wh o ca n drin k quantitie s o f alcoho l withou t apparen t ill-effec t
shows reliabl y his or he r goo d physica l condition ; on e i n poor conditio n woul d
get visibly drunk. Laborers who do hard physical work are notoriously heavy drinkers in many societies.
In sum , we think tha t a worker servin g the colon y collect s quee n pheromon e
in exchange for her services. Since the capacity of a bee to carry queen pheromon e
depends o n her being in good physical shape, the pheromone is a reliable indicator
both of her ability to acquire pheromone an d of her current bodily condition. He r
tolerance fo r pheromone i s evident t o he r comrades , and a s threats do, i t allow s
her t o exhibi t he r abilit y and achiev e her end s wit h les s actua l violence. In fact ,
possessing the pheromone generall y makes even overt threats unnecessary. Moreover, we wonder whether the very act of working for the hive increases the worker's
ability t o carr y pheromone, jus t as , afte r a yea r o f constructio n work , a colleg e
student may "hold his liquor" better than he did in his fraternity-party days.
The suggestio n that quee n pheromon e i s the handicapping signa l that proves
rank an d prestig e i n a large hive or colony , and tha t a worker's capacit y to carry
queen pheromon e reflect s he r qualit y both a s a partne r an d a s a rival , is stil l a
162
164
argument can be illustrated by a variation on his story about the drowning brother.
Let's assum e that instead o f two brothers walkin g by the riverside , we have three
or four . On e o f them fall s int o th e river , and anothe r jump s in to sav e him. Th e
others stan d by , doing nothing . Al l brothers wil l receive the sam e genetic gai n if
the rescu e is successful; bu t th e rescue r risk s injury o r even death , while th e one s
standing by risk nothingtha t is, the slackers ' tota l gai n wil l be greater . The
altruist, then, will benefit less than a selfish brother , an d o n average , the numbe r
of altruisti c genes in the nex t generation will decrease rather than increase .
Motro an d Eshel formulated a mathematical model t o solve this dilemma, but
they di d s o by adoptin g a n unrealistic premise : tha t n o brothe r ca n assume that
another brothe r wil l jum p i n th e wate r i f h e himsel f refrain s fro m doin g so. 32
According t o th e theor y o f kin selection , w e would predic t tha t eac h woul d en courage his brothers to jump in rather than jumping in himself. In reality, we know
it is much likelier that all the brothers wil l jump in to sav e their drownin g sibling ,
and tha t eac h wil l d o hi s utmost t o tak e on th e ris k an d perfor m th e rescue ; n o
brother wil l consider that becaus e the other s ar e struggling to d o the same , he is
risking his genes needlessly .
Thus, grou p selectio n theor y and kin selection theor y have the same flaw: they
invite social parasitism. In fact , ki n selection i s simply group selectio n amon g relatives.33 W e fin d i t strang e that despit e this , man y researchers who rejec t grou p
selection see kin selection a s a viable, stable mechanism, like individual selection. 34
Basing an explanation o f altruism on kin selection theory presents tw o further
problems. Research on group-living birds shows that one or two helpers can indeed
increase the success of a reproducing couple , but tha t more helpers than this have
no effec t o n th e succes s of reproduction. 35 By the logi c o f kin selection , t o invest
in providing unneede d hel p i s a pure loss both to the helpers an d to all their kin .
By that sam e logic, i n fact , al l the helpers ' kin woul d hav e benefited i f these un necessary helper s ha d save d thei r effort s fo r thei r ow n reproductio n o r trie d t o
form ne w groups. Ye t the reproducin g coupl e in group-breeding birds often get s
assistance from mor e helpers tha n they need.
And i f the drivin g force behind th e evolutio n o f altruism is the benefi t gained
by kin, shouldn' t th e sam e logic militat e strongly against aggression toward kin ?
Yet we often se e violent struggle s between ki n collaborators . Indeed , these struggles frequently end with on e or more of the collaborator s bein g wounded o r even
killed. Th e theor y of kin selectio n doe s no t explai n why it is that relative s d o no t
avoid harming each other in their struggles .
Gadagkar an d Josh i describ e a colon y o f wasps tha t spli t int o tw o colonies ;
before the breakup, the level of aggression in the colony was so high that it caused
a sharp decrease in the number o f offspring. Onl y after th e breakup di d the agression subside, an d the number o f offspring the n increased a great deal in both new
colonies.36 As Darwin remarked, it is precisely the social insects that are noted for
excessive enmity to their closest relatives: mother kills daughter, sister kills sister.37
166 TH
ing amon g the m ha d alread y been establishe d th e previou s fall , whe n the y were
living togethe r i n thei r mother' s nest. 41 In th e ne w nest , a division o f labor ap peared: the top quee n staye d in the nest, guarding and taking care of it. The three
sisters next to her in rank went out gathering food. The three lowest-ranking sisters
stayed b y th e nes t withou t takin g par t i n an y activities . Whe n th e to p femal e
disappeared, th e secon d too k it s place an d on e o f the inactiv e sister s joined th e
food gatherers .
This arrangemen t enable s eac h siste r t o fin d ou t wher e he r bes t chanc e t o
succeed lies. The secon d i n rank alread y knows from experienc e tha t sh e canno t
overcome her senio r sister . By going out to collec t food , sh e can meet wasps fro m
other nest s who ar e als o seekin g food. I f sh e finds herself stronge r tha n mos t of
them, there i s a good chanc e sh e coul d protec t a nest effectively . I n tha t case , it
will make sense for her to strik e out on her ow n and establish her own nest .
On th e othe r hand , i f the secon d siste r find s hersel f weake r than othe r foo d
seekerseach o f whom ha s a n eve n stronge r siste r guardin g th e nes t i t come s
fromit will be better for her to go on being a helper an d bring food to her home
nest. In tha t case , her best chanc e will be the possibility tha t her senior siste r will
disappear an d that sh e will take her place in an established nest , with helpers and
possibly workers . A s fo r th e weaker , inactiv e sistersa s lon g a s the y se e thei r
stronger sister s coming back to the nest rather than striking out on their own, there
is little chance that they, being even weaker, would manage alone; there is no poin t
in trying their luc k elsewhere .
West's seve n sisters had known eac h other from th e time they hatched an d had
established a n orde r o f ran k amon g themselve s befor e the y formed th e nes t to gether; the y didn' t nee d t o spen d tim e an d effor t an d ris k injur y t o establis h a
hierarchy a t the beginnin g o f the season , a critical time. We believe , i n fact, tha t
the familiarit y an d establishe d ran k amon g relative s i s th e mai n reaso n fo r th e
prevalence o f coalitions among relatives in the anima l kingdom.
THE KI N EFFECT
There is no doubt that among social animals, other thing s being equal, an individual wh o belongs t o a group whos e member s collaborat e reproduce s bette r tha n
one who belongs t o a group whose members fight each other. This is true even of
collaborations between differen t species , as in symbiosis. I t i s also clear that if for
some reason it makes sense to collaborate with relatives, then in future generations
a scientifi c tall y may sometime s sho w a n increas e i n th e representatio n o f thos e
relatives' genes within the general population. We suggest calling this phenomeno n
"kin effect." 42
Kin effec t i s different fro m ki n selection . I n ki n selectio n theory , the selective
factor tha t drives the evolution o f altruistic traits is the benefit the altruist's relatives
167
gain fro m th e investmen t tha t individual makes in them. By contrast, we say that
altruistic traits evolve by natural selection; that is, they evolve because i n fact the y
improve a n individual' s reproductiv e chances . Investment i n th e grou p benefits
the investo r directly ; ofte n th e gai n t o th e altruis t i s increase d prestige , whic h
facilitates his or her own reproduction. Th e kin effect the impac t these altruisti c
traits may have on the reproductio n of the individual's kincanno t be the facto r
that selects the tendenc y to invest in altruistic acts .
C H A P T E R 1
1 7 O TH
more rarely , the femal e i s the on e wh o goe s of f to fin d anothe r mal e an d leaves
the car e of the offsprin g to the fathero r she may mate with severa l males who
all assist he r i n th e car e of their commo n offspring . I n suc h cases , she practice s
polyandry.
Even whe n raisin g offspring take s both partners, their investment need not be
the same . True, i f one stint s and thei r offsprin g suffer , bot h partner s lose; but if ,
by deserting, on e o f the tw o mates can form a new or a n additional matin g partnership, i t may well gain more than it loses .
But a deserter doe s not necessarily gain. In general it has been foun d that one
is more likel y to successfull y raise a brood wit h a familiar mate , wit h whom on e
has succeeded i n raising offspring before , than by starting over with a new mate.5
Becaused o f the pair' s familiarit y wit h eac h other , the y are probabl y spare d th e
effort o f checking each other ou t and coordinating their actions . Also, research on
songbirds ha s show n tha t youn g hatched earlie r i n th e seaso n ar e usuall y mor e
successful.6 Thu s an individual who deserts its mate and shortchanges their young
may wel l stan d t o los e considerabl y more , i n term s o f it s overal l reproductiv e
success, than i t ca n gain in another partnership ; moreover , ther e is no guarantee
that the deserte r wil l find another partner. 7
cation o f its bearer' s quality . Morton 11 found tha t olde r pair s o f purple martin s
often le t younger pairs settle near them; not infrequently the younger females were
seen copulatin g wit h thei r olde r mal e neighbors. Zilberman 12 observe d sunbird s
in Israel copulating with males, usually their neighbors, who were not their mates.
Extrapair copulation , a s it is termed, turn s out t o be quit e commo n in nature.
Why doe s a female copulate wit h male s other tha n he r mate ? Man y reasons
come to mind. There is the ris k that males from neighborin g territories o r solitary
males will destroy her nest and kill her offspring , forcin g her to lay another round
of eggs in the expectation that they will be the ones to fertilize them.13 To prevent
that fro m happening , th e femal e can tr y t o gai n th e protectio n o f stron g males
living near her, who migh t be willing to shiel d he r offsprin g i n exchange for th e
chance t o fathe r som e o f them . Thi s phenomeno n o f killin g offsprin g was first
observed with langur monkeys in India.14 In Israel, Giora Han i and Yotam Timna
found tha t femal e leopards mat e with severa l males, and that males kill the young
of female s who hav e not copulate d with them. 15
It i s also possible that females mate with additional males in case their chosen
mates are not fertile : by copulating wit h anothe r male, a female raise s her chances
of layin g fertile eggs. She might als o improv e her offsprin g b y copulatin g with a
high-quality male who might not agree to desert his mate for her but is quite willing
to father a few additional offspring o n the side.
In short , a male who pair s up with a female does not necessaril y father all her
offspring. A male who wishes to be sur e that th e offsprin g hi s mate bears ar e his
own ha s t o persuad e th e femal e of his qualit y and o f his willingness to inves t in
her an d i n their commo n offspring , s o that sh e will not tr y or agre e t o copulat e
with other males.
172
the other off the nest. It would seem that this competition ove r caregiving is meant
to demonstrat e th e qualit y and motivation of the caregive r and to strengthe n the
relationship between the parental pair. In fact, when we discuss parasites in chapter
16, we will sugges t tha t by taking car e o f cuckoo chicks , crow s sho w themselve s
off a s good mate s in order t o preven t th e breaku p o f the pair .
Competition ove r th e car e of offspring , lik e th e competitiv e altruis m o f babblers, show s both a n individual's qualit y and it s commitment t o the partnership .
Single males often assis t widows i n raising their offsprin g fo r similar reasons; they
thus prov e thei r qualit y an d th e seriousnes s o f thei r inten t an d increas e thei r
chances t o pai r wit h th e widow s late r on . The widow s ar e desirable mates: the y
have alread y proved themselve s b y havin g offspring. A singl e mal e ma y assis t a
pair t o rais e thei r offsprin g i n orde r t o increas e hi s chance s o f mating with th e
female shoul d he r partne r die . Sometime s th e female' s mate is kicked ou t b y th e
"helper" himself a phenomeno n tha t ha s bee n observe d amon g monogamou s
species as well a s among species that live in groups. 17
An extrem e example o f an anima l proving its
quality by caring for the offsprin g o f others is provided b y fish. In th e Japanese fish Alcichthys alticornis, fertilizatio n occur s withi n th e female' s
body. Afte r th e female's egg s have been fertilized
by one male, she chooses another and lays her eggs
in hi s nest. Onl y afte r sh e has filled his nest wit h
the first male's offspring doe s the female agree to
copulate wit h th e nest' s owner ; sh e then goe s off
with the eggs he has fertilized and lays them in the
nest o f ye t anothe r male . Most male s o f thi s fish
thus tak e car e o f th e offsprin g o f others , a s ha s
been prove d b y DNA analysi s of the offspring. 18
Females prefer males in whose nests there are already large egg deposits; thus, the
investment of each male in others' offsprin g increase s his attractiveness to females.
Indeed, th e females of many fish are attracted to males who are taking care of nests
that contai n plent y of eggs. 19
174 T H
settle for whatever territor y tha t mat e ca n hold. The stronger gender can choose
a partner, o r kick a former partner ou t o f the territory. If he ca n hold a large and
high-quality territory, he may even be able to get an additional female. 23 His greater
strength ofte n allow s him to dominat e the female .
C H A P T E R 1
SOCIAL AMEBA S
(CELLULAR SLIM E MOLDS )
ost scientist s who stud y social system s and communication s i n multicellular organisms ceased long ago to use group selection a s a model
though the y still revert t o that theor y occasionally without realizin g it.
Microbiologists, b y contrast, still routinely use models of group selection to explain
the behavio r of one-celled organisms such as bacteria an d viruses. This approac h
is justified, the y say, because mos t unicellula r organism s reproduce asexually , by
division, an d live in groups that ar e genetically uniform; therefore the populatio n
counts a s a singl e uni t i n term s o f evolution , th e interest s o f it s member s ar e
identical, an d trait s that benefi t th e grou p ar e likely to flourish eve n i f they harm
specific individuals .
But thi s reasonin g ignores th e fac t tha t th e larg e number s o f one-celled indi viduals an d thei r rapi d reproductio n naturall y brin g fort h mutants . Any mutant
that can take advantage of others in the population is likely to increase more rapidly
than thos e othe r cells . W e say , therefore, tha t microorganism s to o hav e t o b e
studied fro m th e poin t o f view of individual selection .
177
178
179
ISO T H
spores. Amebas poor in nutrientsfor example, ones that have just divided, whose
resources are therefore depletedadopt the prestalk type. This effec t i s very pronounced when on e mixes populations o f amebas with artificially altered amounts
of stored nutrients : amebas raised on sugars, and thus rich in nutrients, are much
more likely to become spores than amebas raised on bacteria, which ar e poorer in
nutrientseven though almost 80 percent of each population would have become
spores if each had bee n allowe d t o form a fruiting bod y on its own.
We believe , then , that ameba s forming a slime mold differentiat e b y th e following process. When ameba s gather into a n aggregate, there is no way to tell in
advance ho w eac h wil l compar e wit h others . A s a result, they all behave i n th e
same way: they broadcast their interest in getting togethe r by waves of a chemical
called cAMP, 3 and they all home in on the principal sourc e of those waves. Once
they get together, i t is apparently too late for an y of them to change course. They
cannot leav e an d see k anothe r aggregate , and i t seem s that a t tha t point , thei r
chances on their own are nonexistent. Once ameba s enter an aggregate, their best
chances ar e i n tha t aggregateeve n fo r thos e wh o tur n ou t t o b e les s well nourished tha n others ; the odd s i n the aggregat e might be agains t them, but th e
odds outside it would be worse still.
If th e onl y way to surviv e when foo d i s scarce
were to become a spore in a fruiting body, it would
be pointless for any individual ameba to adopt th e
prestalk strategy . However, nutrient-poo r amebas
have other chances , however unlikely. By joining a
migrating slug , they increase their odds of survival,
since th e "slug " provide s som e protectio n agains t
drying out , an d sinc e i t move s more quickl y than
an ameba can move on its own. One wa y to survive
is to become a spore, an d indeed, as we predicted ,
it ha s recentl y been foundafte r w e forme d ou r
hypothesisthat a few o f the ameba s that star t ou t a s prestalk actuall y end u p
becoming spores. 4
One ca n imagin e other luck y events tha t woul d enabl e a prestalk ameb a t o
survive. The migrating slug may meet with another slug that contains even weaker
amebas. Whe n tha t happens, th e weakes t ameba s i n th e firs t slug , whic h wer e
headed towar d stal k formation, may well end u p amon g the almos t 80 percent of
the combined slug that ar e stronger than the res t an d becom e spores . Moreover ,
the amebas tha t do not become spore s do not necessarily di e right away . As long
as the y are aliv e they have some chance to surviv e if the slu g quickly gets to a n
environment rich in food. For stalk-formin g amebas, these various chances of survival, however slim, are better than the odds would have been had they tried fro m
the outse t t o becom e spore s i n the presenc e o f their stronge r peers . Obviously ,
this subject requires further researc h not onl y in the artificia l environment of petri
dishes in the lab but i n the field.
181
DIP AS A POISON
The differentiatio n of amebas into the prestal k type follows the emissio n of DIP,
a chemica l produced b y the prespor e amebas . And i t is here that ou r hypothesi s
that the slim e mold is a product o f individual rather than group selection becomes
as well a question about th e functio n o f DIP as a signal.
Most scientists consider DIP to be a "signal," which "tells" some of the amebas
that they have to develop int o the prestalk type. Group-selection model s have no
difficulty wit h this: DIP causes some amebas to differentiate int o prestalk amebas,
they say, and thes e prestalk ameba s end u p assistin g the prespore ameba s for the
good of the group. But if one assumes the process evolved by individual selection,
then two questions come up. First, why do the prestalk amebas "obey" the signal
and differentiat e into the prestal k form , a process likely to en d with their death?
Second, why do all prespore ameba s bother to emit DIP? After all , if the amebas
around them are already emitting DIP, a single ameba would still reap the benefi t
of that emission even if it did no t emi t any itselfand i t would save itself the cost
of producin g an d emittin g the DIP . Ho w doe s eac h individual prespore ameba
benefit b y emitting DIP?
DIP eventually causes the prestalk amebas to die; for that reason, we suspected
that it was a harmful chemical a poison. This prediction turne d out to be true. 5
We believe that DIF's poisonous properties are its very reason for being. We think
that the DIP is a poison use d by spores to avoid predation, and that the prespor e
amebas manufacture it for their own individual benefitprobably to protect themselves.
Chemicals that ar e secreted to keep other s awayallelopathi c chemicalsincluding antibiotics, 6 are usually understood t o be a tool that enables a population
resistant to those chemical s to get rid o f populations o f bacteria that are sensitive
to them. This model, again, is based on group selection: any given individual could
save itsel f th e troubl e o f manufacturing the chemica l and rel y instead on th e secretions of others in the population .
We, on the other hand, ask rather how the individual cell benefits by secreting
an antibiotic or a toxin. Perhaps th e antibiotic helps the individual cell protect its
living spac e and it s immediate surroundings against other individual s tha t might
prey o n i t o r caus e it othe r harm . If so , the n althoug h antibiotic s ma y help a n
entire population against another, thi s is not wha t drives the evolutio n o f antibiotics bu t i s rathe r a sid e effect . I n fact , i n natura l populations , th e amoun t of
antibiotics secreted by cells is minute and canno t kill off other populations . Cells
that manufactur e large amount s of antibiotics 6 ar e produced onl y by means of a
strenuous selection proces s conducted b y researchers in the lab.
It i s no t uncommo n fo r microorganism s to us e poison s t o protec t dorman t
spores, whic h woul d otherwis e b e eas y prey. The effor t neede d t o produc e th e
poisons, an d th e dange r an d inconvenienc e the poison s themselve s pose t o th e
pre-spore cell s tha t produc e them , ar e compensate d fo r b y th e protectio n th e
182
poisons provide . W e suspec t tha t thi s is the primar y reason fo r the manufacture
and emissio n o f DIF; th e effec t o n lower-qualit y amebasthe one s wit h fewe r
stored nutrientsi s secondary . If this hypothesis turn s out t o be true , the n DI F
is not a signal but rathe r a straightforward tool. Fo r example , rain causes people
to take cover, but nobod y would sugges t that rain is a signal that appears in order
to cause people to take cover.
Since we suggested thi s hypothesis , Atzmon y and Nanjundia h have found indications throug h bioassay that DIF i s indeed presen t i n spores. 7
If hig h concentration s o f DIF kil l amebas , lower concentration s ar e probably
harmful a s well. The use of DIF force s amebas to devote resources to surviving its
influence and breaking it down. In weaker amebas, we believe, these efforts create
the prestal k phenotype , whic h increases thes e amebas ' abilit y to surviv e the poison's influence in the short term; we have suggested that by trying to form a spore,
a weaker ameba actuall y reduces its chance s of survival, and i t is the presenc e of
DIF more than anything else that creates this stark reality. Collaboration i s crucial
to all the amebasif they don't for m th e slug none will surviveand that is what
makes it possible for the stronge r ones , thos e that can withstand the poison and
form spores , t o exploit the weaker ones.
Cellular slim e molds ar e not unique . Myxobacteria ,
too, for m communa l fruiting bodie s fo r their spore s i n
reaction to hunger. 8 In the process of forming the fruit ing body, some 80 percent o f the cell s are killed by fatty
acids emitted by the bacteria themselves; apparently the
stronger bacteria emit the fatty acids and kill the weaker
in th e proces s o f becoming spores . I n thi s case too, i t
seems t o us , i t i s because collaboratio n i s necessary t o
all that stronger individual s are able to exploit weaker ones; again, to understan d
the process, we have to understand how each spore-forming bacterium cell benefits
by emitting the specia l fatty acid s that kill its comrades. 9
183
184
C H A P T E R 1
PARASITE AN D HOS T
hen a parasite attache s itself to a new host species, both species rapidly
develop new traits. The parasite tries to exploit th e host as much as it
can, and the host tries to protec t itsel f agains t the parasite . Dawkin s
and Kreb s compared thi s relationship t o a n arms race between tw o superpowers,
with eac h manufacturing ne w and mor e sophisticate d weapon s t o counte r thos e
the other develops,1 and it is common fo r scientists nowadays to portray hosts and
parasites as being in the midst o f such an arms race.
We se e things differently . Ther e ar e undoubtedly "arm s races, " bu t w e think
they quickly reach a stalemate. We begi n b y assuming that unles s there is a specific reaso n t o think otherwise , mos t host-parasite systems that exist today are in
a state o f equilibrium: howeve r hard i t may have tried, the host has not manage d
to ge t ri d o f the parasite , an d obviousl y the parasit e has not exploite d th e hos t
to extinction . T o understan d thi s balanc e i n eac h particula r case , on e need s a
thorough, detaile d knowledg e o f the live s o f both hos t an d parasite . What i s it
that stop s the host fro m evolvin g the ability to prevent th e parasite from exploit ing it? What i s it tha t prevent th e parasite from exploitin g eac h host t o the point
of zer o reproduction , o r fro m exploitin g mor e tha n a certai n percentag e o f it s
potential hosts?
185
186 TH
187
reed warbler s who arriv e at their breeding are a later, most of whom d o not rejec t
cuckoo eggs , have ver y worn tai l feathers . Bot h th e stat e o f their tail s an d thei r
late arrival indicate tha t they are young, and tha t thi s is their first year of nesting.
What differenc e doe s age make? The eggs of reed warblers, like the eggs of many bird species, vary; each female
lays eggs that hav e their ow n distinct color , pattern, an d
shape. Som e ar e darker, other s lighter ; some have larger
spots, other s fin e dots . Cucko o egg s may look lik e ree d
warbler egg s generally, but the y cannot loo k exactl y like
the egg s of a specific femal e ree d warbler. 3
Lotem suggest s tha t a ree d warble r wh o ha s neste d
before ha s learned t o recogniz e her ow n eggs and s o can
safely reject cuckoo eggs; inexperienced reed warblers, on
the other hand , cannot . If they were to reject any egg that
looked suspicious , the y might inadvertently destroy their
own eggswhich is apparently a greater ris k than th e 5to-20-percent chanc e tha t the y wil l fal l victi m t o a cucko o i n tha t firs t nesting .
Lotem conducte d experiment s tha t showe d tha t indee d ree d warbler s lear n to
recognize thei r ow n eggs. The relationshi p betwee n ree d warblers an d cuckoo s is
thus no t a n ongoin g arm s race , i n whic h som e warbler s ar e a t a disadvantag e
because the y "haven' t yet " acquire d a geneti c trai t enablin g the m t o ge t ri d of
cuckoo eggs ; rather , the y have reache d a n equilibriu m i n whic h eac h individua l
does th e best it can to succee d i n reproduction .
Of course, on e still has to explain why reed warblers who don't destroy cuckoo
eggs take care of the cuckoo's nestling after i t is hatched.4 The parent warbler doe s
this both i n the nest an d ou t o f it, for some four t o five weeks, by which time th e
young cuckoo' s size , shape , color , an d call s ar e al l very differen t fro m thos e o f
reed warble r nesdings .
188 TH
distinguish between differen t food s a s well as between differen t people , and they
recognize enemies . On e woul d thin k tha t crow s coul d increas e thei r breedin g
success a great deal by learning to discriminate between their own eggs and cuckoo
eggs and gettin g ri d o f the latter . But they don't d o this. A common explanatio n
is that cuckoo s hav e just starte d parasitizin g crows, and th e crow s "haven' t yet "
evolved the ability to fight against them. But we think this is unlikely. Great spotted
cuckoos parasitiz e various population s an d specie s o f th e cro w family (Corvids )
all over Asi a and Nort h Africa , an d throughou t thi s larg e regio n n o populatio n
shows any resistance to them, with one exception: magpies in Spain. Many magpies
in Spai n reject eggs of the grea t spotted cuckoo , bu t no t al l of them do. 6 We ca n
think of two alternative models that can explain the constraints that prevent crows
from resistin g cuckoos: the prestige mode l an d the Mafia 7 model .
ents an d thus stay together. I f they do not brea k up , the y stand a good chanc e of
having a fully successfu l nes t next time. If they "divorce," on the other hand, each
partner woul d hav e t o fin d a ne w mat e an d migh t fai l altogether ; a t best , eac h
would b e likely to have difficulty raisin g offspring nex t yea r as well.
Fledgling cuckoo s tha t com e ou t o f crows' nest s behave as though the y know
that the onl y reason thei r hosts take care of them is to gain prestige. They beg for
food ver y loudly an d pursu e thei r host-parents fa r mor e aggressivel y than thei r
crow nestmates. Rather than try to imitate the crow nestlings' behavior, the young
cuckoos stand out by noisily importuning. We believe that the crows' real offspring
don't nee d to beg as much, since their parents derive a direct reproductive benefi t
from feedin g them . Bu t th e cro w doe s no t gai n th e sam e way from feedin g th e
cuckoo, of course; the only gain it gets from feeding that "pest" is proving to other
crowsincluding its matehow good a provider it is. Thus, th e cuckoo nestling
has to draw others' attentio n to the act of parenting in order to get fed. Of course,
this noisy behavior is dangerous: the young cuckoo is more likely to be noticed by
predators. Thi s ris k is the price i t has to pay for its food.
Needless t o say , we woul d no t drea m o f assertin g tha t th e cucko o an d th e
crows ar e awar e of an d consciousl y calculat e al l thes e factor s of ris k an d gain .
Rather, fledglings who strik e the best balanc e between risk y begging and making
do without begging are more likely to grow up, become successful adults, and have
offspring wh o will spread their traits in the population. Similarly, adult crows who
invest th e righ t amoun t in convincing other s of their qualit y as providers ar e th e
ones mor e likel y to fin d an d kee p bette r mate s an d t o hav e more successfu l offspring. Ultimately, as with any trait, cos t an d gai n must be balancedand young
cuckoos hav e t o inves t mor e i n beggin g tha n youn g crow s do , i n orde r t o ge t
sufficient car e out o f their host-parents.
1 9O TH
192 T H
makes sense for song sparrows to expose their nests to her early, so that the parasite
will lay in their nest s rather than destro y all their eggs .
Thus i t seem s tha t olde r son g sparrow s wh o mo b th e cowbir d an d thereb y
reveal their nests ' locatio n woul d rathe r accep t a certain amoun t of damage than
pay a heavier pric e fo r attemptin g t o evad e o r rejec t the parasite . If th e damag e
caused b y th e on e foreig n nestlin g i s not to o great , an d i f i t i s bette r fo r son g
sparrows to fledge offspring earl y in the season rather than later, as is the case with
many birds , then i t seem s that son g sparrow s wh o mo b cowbird s ar e using th e
best strateg y available to the m when cowbird s ar e present, a s in western Canad a
today. Why, then , don' t younger female sparrow s mo b cowbirds ? I t ma y be that
they are not abl e to rais e both thei r ow n young and the parasite' s nestling. Thei r
only recourse i s to lie low and hope th e cowbir d wil l miss them.
In ou r opinion , th e coexistenc e o f parasites an d host s ofte n depend s o n th e
fact tha t a host stand s t o lose more in an all-out struggl e with the parasit e than it
loses b y toleratin g th e curren t leve l o f parasitism . I n eac h cas e th e resul t i s a
dynamic balance, an d an y change in conditionsan y weighting o f the scale s on
one side or the othermigh t jar it out o f equilibrium.
brings to the mai n nest as food for her own and her host' s offspring . The parasite protects he r mai n nes t agains t other robbers , a very real benefit t o th e host .
Schwammberger found that the presence of this parasite was beneficial to the host.
True, whe n a t the en d o f the seaso n h e compare d th e succes s o f nonparasitize d
colonies wit h thos e tha t ha d thi s parasite , the forme r produce d mor e offspring .
But whe n h e took int o accoun t al l the colonie s tha t faile d durin g th e season , h e
found tha t th e chance s that a nest would surviv e were much higher i f it had suc h
a parasiti c collaborator. I t turn s ou t tha t th e parasit e provide s crucia l hel p earl y
in th e season , when th e hos t doe s no t ye t have daughter s t o shar e the load : b y
protecting the nest, the parasite enables the host to undertake longer hunting trips.
In fact , i n this case the parasite fulfill s th e function same-specie s cofounders do in
other species .
Sometimes a host ca n choose amon g parasites and pic k th e on e least likel y to
damage it; that one might even protect it against the others. As we saw above, this
is a logical outcome of the Mafia model and can lead to symbiosis between species ,
like the partnership betwee n human s and dogs . Whe n i n distant prehistori c day s
humans starte d bringin g foo d t o thei r camp s and storin g it , rodent s an d insect s
started gathering there, and in their wake predators that lived both on the humans'
leftovers an d on the rodents an d insects they attracted. Among these larger predators was the wolf, who, because of its preexisting social traits, was easily integrated
into human society.
The human-allie d wolf refraine d fro m preyin g on weaker
humans suc h a s young children an d chase d other predators ,
including other wolves, away from th e territory it shared with
the human beings. In exchange, the humans shared their food
with th e wolf-dogs . A do g fe d b y humans has a n advantage
over it s wild kin : i t is protected an d fe d an d thu s ca n affor d
to becom e large r an d to tak e risk s in fights that i t coul d no t
afford t o take if it had t o find food or catc h prey on its own .
By cooperating with humans and feeding at its owner's table,
the do g gave up som e of its ability to live independently .
194 TH
over its host's head . Th e bacterium tha t causes diphtheria exist s in the throats of
most human s in a nonvirulent form . A toxin gen e resides in plasmids insid e th e
bacterium,20 whic h ca n manufactur e a killing toxin ; bu t i n mos t case s a special
represser protein, manufacture d by a gene in the bacterium's chromosome, keeps
the bacterium's toxi n gene inactive.
To manufactur e the represse r protein , th e bacteriu m need s iro n tha t i t gets
from it s huma n host . Whe n th e bacteriu m doe s no t ge t enoug h iron , i t stop s
manufacturing th e represser protein, an d the plasmids star t producing th e diph theria toxin , causin g th e deadl y disease . A s lon g a s the bacteriu m receive s th e
nutrients it needsincluding ironit does not produce th e toxin, so it is worthwhile for a human body that can spare them to discharge some nutrients to supply
the bacteria. The bacterium thus "blackmails" it s host int o supporting it .
What doe s the individual bacterium gain from emittin g the toxin? The starved
bacterium ca n probably feed on nearby body cells the toxin disintegrates; perhaps
the toxi n als o protect s th e starve d bacteriu m agains t othe r diphtheri a bacill i
nearby, who are just as starved as it is (see the discusssion on antibiotics i n chapter
14). I f the host does not cooperate, it is to the parasite's advantage to act virulently;
it is only the host's suppor t tha t enables th e nonvirulent phenotyp e t o overcom e
the virulent one .
In diphtheria , thi s tria d o f host , nonvirulen t parasite , an d virulen t parasit e
involves differen t phenotype s rathe r tha n differen t
genotypes o f the parasite . I t ma y well b e tha t similar
relationships occur between host s and various strains,
or genotypes, of fungi, bacteria, or viruses, some more
virulent an d som e les s so . Her e again , th e hos t ca n
assist th e nonvirulen t parasit e an d us e it a s a partner
against its virulent relative. Reliable communication is
as necessary between such partners as it is between any
others.
sumption that what we see today is a dynamic state of equilibrium, a balance that
results because each party is doing its best t o reproduc e a s successfully a s it can.
In case s where w e do no t understan d thi s equilibrium , we assum e that w e have
not yet found all the element s of it, and that we have to look for the missing ones.
Just a s the assumptio n that animal communication is necessarily reliable open s
one's eyes to the richness of communication actuall y taking place in nature, so also
the assumptio n that social system s are in a state of equilibrium enable s one to see
and appreciat e th e incredibl e complexit y an d beaut y o f thes e systems . This ap proach lead s u s to as k new question s an d devis e new hypotheses t o test , an d so
ultimately it turns ou t t o be far more fruitful tha n its alternative.
C H A P T E R 1
INFORMATION CENTER S
198 TH
members o f one flock with colore d le g rings. When w e then presente d tha t floc k
with small heaps of food, eac h heap was taken over by one individual, who chased
others awa y from it . Bu t when w e scattered on e suc h hea p ove r a larger area , an
individual coul d n o longer defen d it effectively; h e stopped trying to and fed side
by sid e wit h others . Whe n w e stoppe d supplyin g food , al l the bird s wh o hel d
territories wen t bac k t o the flock. As far a s we know, it was the first time that an
experiment i n the field showed tha t environmenta l factors can chang e socia l behavior.
As much a s the socia l behavior o f individual wagtail s varies, these birds hav e
one thin g i n common : ever y evening, al l wagtails gathe r i n communa l roosts
sometimes thousands of them together. Bot h flocks and territor y holder s congre gate in the roosts, and some flocks fly fifteen to twenty miles to join them.
Information Centers 1 9
small groups , o n th e othe r hand , i s generally spread sparsel y over larg e area s in
quantities tha t d o no t suffic e fo r mor e tha n a few. For suc h species, ther e i s no
point i n following others to a food source, and thus no point in communal roosts.5
Since w e firs t publishe d th e ide a tha t communa l
roosts serv e a s "informatio n centers " i n 1973 , man y
studies an d experiment s tha t suppor t i t hav e bee n
done.6 Th e theor y is now widely accepted. Brow n ob served swallows coming to their nests in nesting colonies
with food in their beaks , and othe r swallow s followin g
them when the y went back t o get more food. 7 Heinric h
studied crow s i n th e northeaster n Unite d States. 8 I n
winter, thes e crow s fee d o n carcasse s they find on to p
of the snow . When Heinric h pu t suc h carcasses in particular places , h e foun d tha t th e mornin g afte r a singl e cro w discovere d them ,
many crow s cam e to fee d o n them . H e note d tha t thes e bird s flew straight t o a
carcass they had no t know n o f previously; most of them cam e directly from thei r
communal roost, following the roostmat e who had foun d it the da y before.
In our original article on roosts and gatherings, we suggested that all gatherings
of animal s evolved t o provid e individual s with informatio n abou t foo d sources .
Today it is clear that som e gatherings provide other benefits.9 Animals also gather
to find mates: the communa l leks of ruffs an d o f black grous e that were describe d
in chapte r 3 hol d hundreds , sometime s eve n thousands , o f birds , an d th e larg e
concentration o f males enables female s to choose the best of them. Wagner found
that razorbills a monogamou s bir d specie s i n whic h bot h mate s tak e car e of
offspringgather i n special mating arenas to copulat e both with their mate s and
with other s (extra-pai r copulation). It woul d mak e sense that gatherin g togethe r
in breedin g colonie s an d i n communa l roosts, whether durin g th e da y or fo r th e
night, also gives birds the opportunity to get to know potential mates and thus to
choose thei r mate s better , thoug h ther e i s no proo f o f tha t yet . Som e breedin g
colonies primaril y offer protectio n fro m predators , an d ye t other gatherings, usually small ones, enable individuals to pool their bod y warmth on cold nights. 10
There ar e man y additional example s o f information centers . Sandgrouse , for
instance, ar e bird s o f th e stepp e an d desert ; they ar e abou t th e siz e o f pigeons ,
and the y ea t grain s an d greenery , which ar e distribute d ver y unevenl y i n thei r
desert habitat . I n th e summe r they fly large distances t o source s o f water. Som e
species drin k in the morning, about a n hour after sunrise , and others drink in the
evening. The sandgrouse come to the water sources in couples or small flocks; once
there, however , the y gather int o large flocks and spend tim e together chattering ,
chasing each other, courting, an d preening thei r feathers. They are very cryptic in
color, an d th e flock looks lik e a field of stoneswhich suddenl y turn int o bird s
when they rise and fly together t o the water. When th e sandgrouse rise up in flight
they are visible an d audible a t a great distance. No doub t these gatherings, which
can be seen in several places in Israel's Negev desert, serve as information centers.11
2OO TH
E H A N D I C A P P R I N C I P L E I N SOCIA L SYSTEM S
Information Centers 2O
cover it , doesn't las t long, and they are widely scattered; by the tim e kites gathe r
in the night roost, carcasses found that day have already been eaten. Even so, most
kites leave their communa l night roost together an d fly over the marshes and sand
dunes in a scattered flock. Once a kite finds a carcass, the other s joi n it and fight
over it .
Interestingly enough , the flock the researchers observe d wa s composed mostl y
of migratory , wintering kites . Local kites , wh o kne w th e are a well, di d no t a s a
rule come to the roost an d did not join the flock but rathe r went out on their own,
usually in their regula r territories. Th e researcher s also found that kite s tha t had
fed well the previous da y also preferred to strike out on their own, apart from th e
flock.
A group o f kites can find an isolated chicke n carcas s more easily than a single
individual can . But once a carcass is discovered, its finder has to fight for it. Very
hungry kites, for whom eve n a mouthful would mak e a difference, d o no t hav e a
choice: the y g o with th e flock , whic h i s likelier t o brin g the m t o a food sourc e
sooner, eve n a t the pric e o f having to struggl e at that point with their flockmates
to ea t some of it.
On th e other hand, a kite who knows the area well or who is well fed can affor d
to search longer an d then ea t at its leisure, far from othe r kites. Only if it does not
find food ove r a stretch o f days would i t benefit from joinin g the flock. The com munal roost, then, enable s kites to search fo r food in a group when the y need to ;
in addition, by checking the number of other kites who join the flocks, an individual ca n estimate ho w abundan t foo d i s i n th e genera l area . I t ca n the n decid e
whether to stay or move on to another region.
2O2 TH
Information Centers 2O
if they dry up later; finding new ones will be difficul t o n its own or in a small flock.
In unfamiliar places, large flocks that cover wide areas can find food more easily
especially i f some members of the flock know the are a from years past.
Bucher recentl y suggested that th e famou s passenger pigeon (Ectopistes migmtorius) becam e extinc t partl y because it s traditiona l roost s wer e disrupte d b y
hunting and development, and the reduced populations could not gather the information the y needed t o fin d th e mas t crops o f breech trees , th e scattere d an d
unpredictable foo d supply on which they depended.14
Wynne-Edwards describe d th e gatherin g o f bird s i n communa l night roost s
and suggested that such roosts evolved in order to enable a population of birds to
spread itsel f over a n are a according to th e distributio n o f food i n it. We d o no t
accept Wynne-Edwards's explanatio n o f the evolutio n o f communal night roosts,
but i t should be noted tha t the collective information in these centers does indee d
indirectly help adjus t th e distributio n of birds accordin g to food distribution. 15
HUMAN GATHERINGS
Human gatherings , too, serv e a s information centers . Immanue l Marx followe d
festive gatherings (zaharas) at saints' tombs among Bedouins in the Sinai Desert.16
He foun d tha t whe n th e politica l situatio n was stable, fe w came to suc h gatherings; when condition s were volatile an d th e futur e uncertain , the numbe r o f participants ros e markedly . Whether o r no t i t i s the mai n reaso n th e festivitie s are
held, i t i s clear that on e functio n o f the gatherin g is to provid e participant s with
information.
Amotz himsel f foun d ou t ho w beneficia l communal praye r ca n be . H e wa s
called u p fo r arm y reserve duty. None o f the soldier s in his unit kne w what they
had bee n summone d for , where the y were going , what the y would d o there , o r
when the y would b e released . Th e uni t was taken in the dar k of night to a n unknown location , an d the soldier s went to sleep . I n the morning, the pious among
them ros e earl y an d wen t t o prayer , whil e th e other s staye d i n bed fo r anothe r
precious half-hour.
Amotz wok e u p amon g the latter , who wer e al l as clueless a s they had bee n
the previou s night. But the guy s coming bac k from morning praye r knew everything. The congregatio n had include d me n from othe r unit s a s wellmilitary intelligence, transportation , operations , an d s o onan d chat s befor e an d afte r
prayers lef t th e devou t full y informe d abou t th e unit' s prospects . Th e nee d fo r
knowledge i s on e o f th e majo r reason s peopl e gathe r i n clubs , pubs , an d othe r
places17even though what gets a person out o f his or her house may be the wish
to go to a sporting event, watch birds, have a drink, or fulfill religiou s obligations .
Veblen, who lived at the end of the nineteenth century , explained why printing
2O4 TH
press workers were particularly kee n on drinking contests at that time: they had a
specialized skil l that with the rapi d expansion of publishing was in great demand,
and thus they could move from on e place to another an d work for whoever would
pay th e most . Thes e wanderin g workers made transient connection s wit h peopl e
they ha d no t know n before , wh o wer e thei r professiona l peer s an d occasiona l
competitors. B y drinking together, the y coul d ge t to kno w eac h othe r an d brag
about thei r abilitie s to their ne w friends. Thus , bars enabled eac h to establish his
social an d professiona l statu s and probably als o served as information centers for
those seekin g work.18
Information Centers
205
It i s difficul t fo r researcher s t o follo w individua l behavior i n a huge congre gation o f birds. Onl y whe n technolog y enable s u s to mar k many individuals an d
track them closel y within suc h a large gathering will we begin t o understand th e
mechanics o f flocks better. Still, we believe tha t individuals in flocks and in roosts
are aware of each other's doings , and that many of them know and remember one
another. Althoug h w e don' t kno w exactl y how individual s benefi t fro m calling ,
performing aeria l maneuvers, and s o on, we do think it possible tha t showin g off
"in public " increase s an individual's prestig e in flocks and communa l roosts a s it
does in other interactions among animals . A s always, we are guided by the logic
of individual selectioneven when seeking to understand remarkable phenomena
of collectiv e social activit y like roosts and flocks .
P A R T I
HUMANS
C H A P T E R1
HUMANS
uman social life, like that of all other organisms, reflects the interaction of
cooperation an d competition among collaborators. We don't mean to suggest that human social systems are not vastl y more complex tha n those of
animals. Still, we believe that the same principles guide both; the behavioral mechanisms tha t surviv e ove r generation s ar e thos e tha t increas e th e numbe r o f th e
individual's childbearin g offspring. Thus, we will be guided by the Handicap Principle as we examine the logic behind mechanisms of social behavior an d method s
of communication amon g humans.
Some people objec t when human behavior i s compared to that of animals. Yet
we do this routinel y in human physiology. Research on the heart an d circulator y
systems, the kidneys, and the immunological systems of animals has taught science
a great dea l about th e functioning o f the human body. Why, then, should we not
seek the sam e kinds of insights when we consider bod y parts and traits that serve
social purposes?
2O9
21O HUMAN
Humans 21
212 HUMAN
Humans 2 1
214 HUMAN
Menstruation
Body processes , too , ca n be signals ; a case in point i s menstruation. Women ar e
unique among mammal s i n the amoun t o f blood an d body tissue they discharg e
every mont h i n thei r menstrua l flow . Thi s i s no t require d fo r fertility , fo r mos t
mammals conceive without it. What, then, is its purpose ?
Menstruation i s a reliable indicato r o f a woman's physical condition. Whe n a
woman is sick, either bodily or mentally, or when she expends great physical effort,
as in sports competitions, he r menstruation may cease or become disordered. Preg nancy stops menstruation. Menstruation thus informs a woman's mate or potentia l
Humans 2 1
Clothing
We sa w in chapte r 4 how animals ' marking s accentuate bod y part s or trait s that
are important t o othe r members o f their species . Th e sam e can be sai d of much
human decoration . Clothing , especiall y when no t neede d fo r protectio n agains t
cold, wind, o r sun , is used a s decoration an d fo r showin g off. Like the markings
of animals , style s o f clothing evolve whe n member s of a set compete to show off
their quality in areas important to that group. The styles that evolve emphasize the
points of beauty, proper conduct, and economics that are important to the set and
enable observers to compare one member o f the set with another. People who do
216 H U M A N
not bothe r t o dres s accordin g t o th e cod e o f their se t ar e als o showin g off : the
message may be that they do not belong to the group and do not care to be judged
by it s standards , o r tha t thei r strength s can b e effectivel y displaye d eve n i f they
don't conform to a dress code.
Ever sinc e propert y becam e a n importan t criterio n o f socia l success , clothe s
have serve d t o sho w of f wealthwhether the y ar e mad e o f expensiv e materials
or requir e a lot of skilled work. Lately, modern productio n technique s hav e lowered th e cos t o f clothing t o suc h a n exten t tha t i t is difficul t fo r most t o tel l th e
difference betwee n expensiv e clothing and imitations. Designer label s are no help,
since they are absurdly easy to imitate. It seem s that now, more than a t any other
time i n hundred s o f years , clothes ar e becomin g les s importan t i n showin g off.
Instead, peopl e show of f their bodies , wit h shor t clothing , cutoffs , an d revealin g
necklines.
Sometimes standard s in clothin g ar e imposed fro m above , a s is the cas e with
army or school uniforms. Of course, such prescribed clothin g does not reflec t th e
personal tast e o r wealth o f its wearers, but i t enable s superior s an d commander s
to asses s differences i n personality traits that are important to them, such as neatness an d precision . Thes e trait s are reflected by the wa y a uniform is maintained
and worn, an d the y are easier to evaluat e precisely because th e individuals bein g
compared al l wear the same uniform. For th e same reason, the first few months at
the Israeli ai r force's school of aviation are devoted t o drills, polishing equipment ,
and precis e maintenanc e o f one' s uniform . These activities , which ma y seem t o
have nothin g to do wit h flight , in fac t test eac h would-b e pilo t wit h regar d to
personality trait s that ar e critical t o hi s or her commandersorderliness , obedience, and precis e executio n o f commands .
Clothing an d othe r decoratio n modifie s or enhances signal s that are conveyed
by specifi c part s o f the huma n body . Th e neck , fo r example , support s th e hea d
and has to bear its weight. The longer the neckprovided it is also strong enough
to support th e head properlythe more one is able to move the head aroun d and
the bette r us e one ca n make of sensory apparatus in the head . Me n have neede d
a stron g nec k fo r fighting , however , an d therefor e coul d no t affor d a long, thi n
neck. But women ar e not usuall y fighters and ca n afford t o possess and sho w off
a longer neck.
Women, especiall y young ones, often decorat e their necks
with close-fittin g necklace s o r ribbons . A lin e acros s a lon g
structure makes it appear shorte r than it really is, so it is precisely a long nec k tha t on e ca n advertis e reliabl y b y tyin g a
ribbon aroun d it ; th e perso n wh o wear s the ribbo n i s proclaiming that , despit e th e handica p sh e imposes o n herself ,
her nec k ca n be see n to be longer tha n those of her compet itors. A girl with a short neck canno t afford t o wear a ribbon;
such decoratio n woul d mak e he r appea r ridiculousl y
short-necked.
Humans 2 1
218 HUMAN
Humans 2 1
22O HUMAN
men an d women, which produce children ; and thos e between same-se x partners,
which hel p sustai n an d enhanc e companionship s o f various sorts . I n bot h cases
the sexua l act can serve as a mechanism that lets the partners test the partnershi p
and sustai n it. Just a s sex between me n an d women encompasse s more than procreation an d serve s als o to tes t th e bon d betwee n them , se x can provid e infor mation neede d t o maintai n bonds betwee n partner s o f the sam e gender. Again,
this is not uniqu e t o humans : Trivers describe s pair s of female wester n gull s behaving a s perfectl y norma l couple s an d togethe r raisin g offsprin g conceive d
through extrapai r copulation.14
Of course , the sexual act is not necessarily enjoyable to both participants. Just
as consideratio n an d car e for one' s partne r ca n be demonstrate d throug h sex , so
can th e lac k o f it . An d tha t lac k o f consideratio n elicit s another messag e in re sponse: one who continues to accept such treatment is telling the other very clearly
that, unsatisfactory as the relationshi p is , he or sh e does not wan t to end it . That
may b e becaus e o f other perceive d benefit s tha t see m more important tha n care
and consideration , or because of a lack of alternatives.
Forced sexrapei s ofte n use d a s a means o f crud e dominance . Thi s i s as
true amon g me n a s between me n an d women . Again , mounting s a s a means of
showing dominanc e are no t a t al l uncommon i n th e anima l kingdom, eithe r be tween male s an d female s o r amon g males: this has been show n in numerous species.15 And all human languages, it would seem, have some verb that takes on both
the sexua l and the dominativ e meanings of the colloquia l America n English ver b
"to scre w (someone)."
The sexua l ac t amon g humans show s reliabl y the qualit y o f the relationshi p
between those participating in it. Between caring and devoted partners, it expresses
that car e and devotion . A n uncaring partner will find it hard to hid e th e lac k of
carewhich ma y lead th e other member of the pair to leave. The sex act may be
used t o prov e th e other' s helplessnes s an d powerlessness , a s in rape . We will let
novelists an d poet s detail th e peak s an d abysse s of the huma n sexual act, and all
the levels in between. Our poin t here is a global one: that it is precisely the closeness an d invasivenes s of the ac t tha t make it a means of conveying and receivin g
detailed an d reliabl e informatio n about th e characte r of its participants an d their
relationship with eac h other.
Humans 2 2
jump at a parent are forcing their parent to catch them. Similarly, women throwing
themselves int o thei r lovers ' arm s coul d b e badl y bruise d i f th e lover s di d no t
receive them . Al l ar e endangerin g themselvesmos t probabl y unconsciously
and a s a result, they get information the y would no t hav e gotten otherwise ; the y
are testin g the socia l bond . The ris k itsel f force s th e othe r part y to com e to th e
tester's ai d and thus to express commitment.
Suicide i s a n extrem e case . On e coul d eve n redefin e successfu l suicide s a s
unsuccessful call s for help. More often tha n not, however, death is not th e result,
and the suicid e attemp t cause s friends an d famil y t o give the desperat e risk-taker
help tha t was not forthcomin g before. Th e person wh o attempts suicid e may not
be awar e of this logic: he o r sh e may honestly prefer deat h t o a n unbearable life .
Such a n attemp t a t suicid e i s genuine, an d tha t i n itsel f convince s other s o f th e
need t o help. Sometimes the perso n attemptin g suicide may even be half awar e of
this logic, a s when someone take s an overdose o f sleeping pills, then call s a friend
and says , "I f yo u don' t com e an d sav e me, I' m dead. " Th e ris k i s still genuine ,
though, an d i t doe s forc e th e frien d t o com e an d help . Th e ris k of death i s what
persuades other s o f how desperate the situatio n isan d indeed, deat h may seem
better than the prospec t o f a hopeless an d helpless life .
222 HUMAN
intensity of the wish is conveyed reliably by the quality of the beggar's voice. When
a babbler threatens , its comrades know without being told who is being threatened,
why, and what the threatene r expects the other t o do ; again, this is obvious fro m
the circumstances. What the y need t o find out is how reliable and how intense th e
threat is. This i s conveyed best an d mos t reliabl y by nonverbal communication .
The informatio n tha t nonverba l vocalization s d o conve y i s ver y exact : the y
express the degree of feelings much more precisely than words can. 19 For example ,
the word s I a m angry d o no t conve y how angr y one is ; to conve y the degre e o f
anger b y word s alone , on e ha s t o us e mor e words : " I a m ver y angry" ; " I a m
somewhat angry. " Even then , words ca n express only a few of the infinit e gradations of anger that are possible; but nonverba l vocalizations reflect such gradations
admirably.
On th e othe r hand , human beings wh o are not familia r wit h on e another may
perceive a give n circumstanc e differently . A perso n listenin g t o a strange r ma y
be unabl e t o relat e th e intensit y of vocalization to th e degre e of emotion, a s the
stranger's constan t companion s can , from pas t experience . Thi s i s especially true
in meeting s betwee n peopl e o f differen t cultures . I n tha t situation , i t i s best t o
communicate with words, eve n if the partie s hav e to us e a dictionary to translate
from on e language to the other . Verbal language may be a poor, inexact medium
for expressin g feeling s an d degree s o f feelingbut i t ca n prevent th e misunderstandings tha t migh t aris e fro m incorrec t interpretatio n o f nonverba l vocaliza tions.
We don' t know how symboli c word languag e evolved i n humans. But once it
did, it enabled group s of humans who were not eac h other's constan t partners to
collaborate temporarily : for protection, fo r war, for hunting. These alliance s were
short-term and required cooperatio n amon g partners who did not work togethe r
most of the time. Such partners also had to be able to discuss things that were not
within viewto say, for example, "There is a saber-toothed tiger on the other side
of this hill," or "Yo u com e up the valley, I'll hid e in the canyo n by the spring. "
People who ar e accustomed t o working together ac t and communicate differ ently than those who d o not a s a rule work together. A regular crew of movers do
not nee d man y words when it comes to carrying a piano up a flight o f stairs. Each
of them knows from experienc e where t o grab, how to carry , when t o push, pull,
lift higher , or stop . All they need is a signal at the instan t they are to lift th e piec e
off th e floor , an d possibl y a few monosyllables a t certain moments alon g the way.
A few short grunt s by the leade r may well be sufficient .
On th e other hand , if a group of people wh o have not worked togethe r before
are calle d upo n t o lif t a heavy item, they will have no choic e but t o discus s each
move in detail before attemptin g i t and t o continu e th e discussio n while carrying
out the task. Even then, their teamwork will be less perfect than that achieved by
the firs t grou p b y means o f a few short grunts . Bu t thi s secon d grou p doe s no t
have enough experience to work as a team with few or no words. Verbal language
is the only tool that ca n enable them t o labor togethe r successfully .
Humans 2 2
224 HUMAN
Humans 225
quality o f materia l an d craf t i n fin e crysta l looks tacky when copie d i n molde d
plastic. Plastic , though , look s beautifu l in design s tha t brin g ou t it s own uniqu e
qualities. Not all have the skill to create such designs and execute them well. People
who d o ar e artist s and talente d craftsperson s who understand an d know how to
work wit h th e materia l the y use . Thi s abilit y coul d hav e beenan d apparentl y
wasappreciated fro m th e ver y startfro m th e firs t tim e a smeared-o n do t o f
colored mu d wa s applied effectively .
226 HUMAN
We certainl y don't assert tha t those who volunteer t o risk themselves i n order
to save another ar e playacting or operating cynically to further thei r own interests.
We have the drive , instilled b y natural selection , t o occasionally risk our live s for
another. Bu t o n average , altruists ar e likely to gai n more tha n the y lose. I n fact ,
self-sacrifice i s no t th e onl y risk y behavio r typica l o f humans . Man y sport s ar e
dangerousauto racin g is a blatant example ; s o ar e suc h pursuit s a s mountai n
climbing, voyaging in space, and exploring unknown parts of the planet. But those
who succee d gai n fame.
Both thos e wh o spen d resource s an d ris k thei r healt h an d lif e fo r fame , an d
altruists who invest resources o r risk health and lif e for their comrades, gai n prestige accordin g t o thei r society' s principle s an d needs . A s a rule , w e accor d thi s
prestige an d respec t a s a matter o f cours e an d d o no t conside r the m t o b e th e
benefits o f altruism. We ar e much more awar e of the cos t of altruism than we are
of the benefi t i t brings t o th e altruist , just a s we are much more awar e of cases in
which a suicid e attemp t result s i n deat h tha n o f th e fa r mor e frequen t case s in
which th e resul t i s that hel p tha t migh t no t hav e been forthcomin g without i t is
made available.
Patriotism i s a form o f "altruism" that is hallowed i n many cultures. An educational syste m that stresse s lov e fo r one' s country , an d th e rea l need t o defen d
that country , can create an atmosphere in which an y attempt t o avoid the dange r
involved bring s a loss of social standing. Yet once one reaches the battlefield, th e
opinion o f one' s comrade s i s th e immediat e motivation . I f on e ask s officer s i n
select combat units what it is that motivates soldiers to risk their lives, they answer
that the strongest drivin g force is shame and the risk that one's comrades will think
one a coward. Even mercenaries take risks in battle, although they don't have such
a stake in the caus e they are fighting for. For them , their comrades ' good opinion
is all that motivates them to take risksand this may be enough t o move them t o
deeds o f heroism.
Gift-giving i s another altruisti c act that increases th e prestige o f the giver . We
are ashamed to give gifts o f lesser value than those we receive. Fo r this reason, we
tend t o give our more prosperous acquaintance s more expensive presents tha n we
give th e les s well-to-do , eve n thoug h th e latte r migh t hav e greate r needs . An d
indeed th e custom of shaming rivals by giving them presents exist s in many human
societies. I t wa s highly developed i n the potlatc h o f the Northwes t Indians : the y
would hol d extravagan t feasts, a t which rivals were presented with expensive gifts ;
a riva l wh o faile d t o retur n i n kin d los t face. 23 I n th e highland s o f Papua Ne w
Guinea, too , som e triba l head s lavis h gift s o n thei r rivals , attemptin g t o giv e so
much tha t th e othe r wil l b e unabl e t o reciprocate . No t fo r nothin g di d th e old
Jewish sage s say that "th e hate r o f gifts shal l live."
Fund-raisers are well aware that donations pledge d o r handed over in the presence o f peers ten d t o b e muc h large r tha n donation s give n i n private . Thi s ha s
become a cornerstone o f Jewish fund-raisin g i n the Unite d States : charit y events
are organized so that donations will be publicized a s much a s possible amon g the
Humans
227
donor's business associates and competitors. Donations are solicited publicly, ofte n
at large meetings, by persons of high status, who themselves contribute hefty sums
and thus "force" others to do likewise s o as not to lose face .
Bakal, who studied charit y in the United States , say s that these methods were
first practiced by Josef Willen. 24 Willen mad e constructiv e us e o f the findings of
the America n sociologis t Veblen , wh o stresse d th e importanc e o f conspicuou s
consumption a s a mean s o f showin g of f economi c status. 25 Afte r all , fro m th e
giver's point o f view, conspicuous donatio n i s simply a form o f conspicuous con sumption: bot h prov e tha t on e ha s mone y to thro w away . Showin g of f one's financial well-being i n a reliable manner has a great deal o f purely practical value;
for example , it can reassure potential busines s partners and facilitate future deals .
The Jewish sage s were wel l awar e tha t donor s gain prestige , just a s they un derstood tha t recipients o f charity lose face; accordin g to Judaism, it is important
to giv e in secret, s o as not t o sham e th e recipient . Thi s doe s not contradic t th e
notion tha t altruism is a means of gaining acclaim. Donors wan t to increase their
prestige no t i n the eye s of those wh o receiv e their charit y but rathe r in th e estimation of their peers, acquaintances, competitors, or mateswho are often aware
of th e donatio n eve n when i t i s supposedly secret . "Secret " donation s ar e made
to protec t th e self-respec t and reputatio n o f the recipient whose estee m is quite
likely unimportant t o the dono r anyway .
When we seem t o pursue ou r own interests, we are considered "selfish" both
by ourselves and by others. O n th e other hand, we believe ou r tendency to act for
others' benefit , which logicall y does no t see m t o be self-serving , i s an expressio n
of "good moral values"; w e feel impelled to follow the path of "altruism," an d we
respect other s fo r followin g it . W e ar e vividl y conscious o f the costs , risks, an d
dangers entailedof th e handicap involvedan d that's precisel y why we are impressed b y altruism. Yet we consider i t bad for m t o calculat e the benefit s it may
bring us.
Still, the sham e we feel whe n w e canno t retur n favor fo r favo r show s that on
some leve l w e are well awar e of the prestig e altruism bring s us , and o f the effec t
this prestige has on our socia l standing. The wisdom of generations acknowledges
that altruis m is indeed rewardedtha t indeed , a s our grandmothe r use d t o say,
"when you do good, you do well."
EPILOGUE
he Handicap Principl e i s a very simple idea: waste can make sense, because
by wasting one proves conclusively that one has enough assets to waste and
more. The investmentth e waste itselfis jus t what makes the advertisement reliable . Thi s ide a seeme d s o obvious t o u s that w e assumed at first that it
must alread y b e widel y accepted , an d s o we searched th e existin g literatur e fo r
discussions of it.
Our searc h yielde d many previous attempt s to explai n th e waste on e sees i n
sexual showing off. Most of these explanations were very complex, and some were
aided by mathematical models, but th e Handicap Principl e wa s not amon g them.
And t o ou r grea t surprise , this idea, which struc k u s a s self-evident, was bitterly
resisted b y the scientifi c establishment . Eve n more to our surprise , this same idea
ended u p revolutionizin g ou r understandin g o f communicatio n throughou t th e
living world, up to an d including communication within the body.
The Handicap Principle states that the receive r o f a signal ha s a stake i n th e
signal's reliability, or accuracy, and will not pa y attention t o it unless it is reliable.
Thus signals are not arbitrary ; rather, each signal is the one best suite d to reliably
convey the specifi c messag e it carries . It follow s that there must be a logical connection betwee n th e message and th e signal . The Handicap Principl e enable s us
229
23O EPILOGU
NOTES
Introduction
1. Zahavi , A., 1975 , 1977 .
2. Davie s and O'Donald, 1976 ; Maynard Smith, 1976b; Kirkpatrick, 1986 .
3. Eshel , 1978a ; Pomiankowski, 1987 .
4. Grafen , 1990a, 1990b .
5. Lotem , 1993a ; Maynard Smith, 1991a; Collins, 1993 .
Chapter 1
1. Se e Maynard Smith, 1965. Th e difficult y wit h group selectio n will be discusse d in
chapter 2.
2. Zahavi , 1978b.
3. Curio , 1978 .
4. Marler , 1955 .
5. Sordal , 1990 .
6. Morri s (1990 ) describe s ho w ma n ha s fro m ancien t time s use d birds ' mobbin g
instincts to hunt them, using decoys of raptors.
231
232 NOTE
7. Car o (1994 ) surveys current studie s of slotting as well a s past explanation s of this
behavior. Se e also Hasson, 1991a.
8. Zahavi , 1977a , 1987 .
9. Fitzgibbo n an d Fanshawe, 1988 ; Caro , 1994 .
10. Hasso n et al, 1989 .
11. Hasso n (199la ) recently reviewed communication s betwee n pre y and predator by
pursuit-deterrent signals.
12. Smythe , 1970 .
13. Rhisiart , 1989 ; Cresswell , 1994 .
14. Wiklun d and Jarvi, 1982 .
15. Ritland , 1991a, 1991b .
16. Eshel , 1988 .
17. Kruuk , 1972 .
18. Eshel , 1978a .
Chapter 2
1. Lorenz , 1966 .
2. Maynar d Smith and Parker, 1976 .
3. Zahavi , 1977a .
4. Ewer , 1968 .
5. Baerend s and Baerends-van Roon, 1950 .
6. Glutton-Broc k et al. , 1982 .
7. Zahavi , 1981b.
8. Morton , 1977 .
9. Zahavi , 1982; see more in chapter 6.
10. Davie s and Halliday , 1978 .
11. Katsir , 1985, 1995 .
12. Se e also chapter 6.
13. Schjelderup-Ebbe , 1992 ; Lorenz , 1966; Marle r and Hamilton, 1966. Se e chapter 12
for furthe r details .
14. Darling , 1937 .
15. Barret e and Vandal , 1990 .
16. Lorenz , 1966 .
17. A detailed discussion of the drawbacks of the model of group selection can be found
in Dawkins (1980). See also Maynard Smith, 1964, 1976a .
18. Lorenz , 1966 ; Wynne-Edwards, 1986. William s (1994) uses a different definitio n of
"group selection " an d stresse s that h e doe s no t assum e the existenc e o f adaptations that
developed "fo r the goo d o f the group."
19. Se e Axelrod, 1986 ; w e will discuss this subject further i n chapter 12 .
Chapter 3
1. Williams , 1966 . Williams' s idea was further develope d by Trivers (1972) who examined its various implications.
Notes 2 3
234 NOTE
value o f feature s b y thei r frequenc y i n a population. Suc h solution s wer e later calle d by
Maynard Smith "evolutionary stable strategy" (ESS) and have been used by him to explain
many other social phenomena. See Maynard Smith, 1976c.
44. Se e Fisher, 1930, 2nd edition (Ne w York: Dover Publications, 1958) , p. 155 : "Th e
possibility shoul d perhap s be born e i n mind i n such studies tha t the most finel y adorne d
males gain some reproductive advantage without the interventio n of female preference, in
a manner analogou s t o that in which advantag e is conferred b y special weapons. The establishment of territorial rights involves frequent disputes, but these are by no means all mortal
combats; th e mos t numerous , and fro m ou r poin t o f view, therefore, the mos t importan t
cases are those in which there is no fight at all, and in which the intruding male is so strongly
impressed o r intimidated by the appearanc e of his antagonist as not t o risk the damag e of
a conflict. As a propagandist the cock behaves as though he knew that it was as advantageous
to impress the males as the females of his species, an d a sprightly bearing with fine feathers
and triumphant song are quite as well adapted for war-propaganda as for courtship." Fisher
has no explanation for this effect, an d continues (p. 156): "The evolutionar y reaction of war
paint upo n thos e who m i t i s intended t o impres s shoul d b e t o mak e the m les s an d less
receptive to all impressions save those arising from genuin e prowess."
45. Se e Alcock, 1993.
46. Andersson , 1994.
47. Zahavi , 1981a , 1987 , 1991a .
Chapter 4
1. Lorenz , 1966 .
2. Wallace , 1889 .
3. Mayr , 1942 .
4. Smith , 1966 , 1967 .
5. Katzir , 1981a , 1981b .
6. Snow , 1976 .
7. Selander , 1972 .
8. Zahavi , 1978, 1981, 1987 , 1992 .
9. Se e more in chapter 5.
10. Barlow , 1972.
11. Zahavi , 1978a, 1981a, 1987 , 1993 .
12. Hailman , 1977; Morris , 1990 .
13. Tinbergen , 1953 .
14. Se e more in chapter 8 about the benefit s an d drawbacks of two colors rather than
one.
15. Hamilto n an d Zuk, 1982.
16. Se e also Hasson, 1991b .
17. Moller , 1990a, 1992 .
18. Watso n and Thornhill, 1994.
19. Thornhill , 1992a , 1992b .
20. Parson , 1990 .
21. Zahavi , 1993 .
22. Se e Zahavi, 1978a.
Notes 2 3
Chapter 5
1. Redond o and Castro , 1992.
2. Eibel-Eibelsfeldt , 1961 .
3. Huxley , 1914 .
4. Cullen , 1966 .
5. Morris , 1957 .
6. Zahavi , 1980, 1987 .
7. Simpson , 1968 .
8. Boake , 1991 .
9. Kreb s and Dawkins , 1984 .
10. Kruuk , 1972 .
11. Th e assumptio n tha t the abilit y to notice signal s precedes th e evolution o f a signal
serves t o explai n wh y animals are sometimes attracte d t o signal s that d o not exis t in thei r
species (Basolo , 1990; Burley , 1986). Ryan (1990 ) describes man y such case s and suggests
that when females are preinclined t o specific sound s o r colors, their sensitivities are utilized
by males who adop t thes e attractiv e features. He term s this phenomenon "sensor y exploi tation." But in our opinion , th e fac t tha t observers ar e able to sens e one signal or anothe r
does no t caus e the signa l to evolv e i n a particular way. Obviously, n o signa l will evolv e if
236 NOTE
the on e signaled cannot perceive it. But neither will it evolve if the receive r finds the infor mation uninterestin g or unreliable .
Chapter 6
1. Zahavi , 1982.
2. Katsi r (1985 , 1991 ) foun d that the inversio n frequency of a babbler cal l is related
to th e stat e o f the bod y making the call : it is very low when th e babble r i s sitting relaxed
on its nest, higher when it is standing in a tree, and higher yet when the babbler i s in flight.
On inversio n frequenc y i n birds and its physiological basis , se e Greenewalt (1986) o n the
physiological side of birdsong .
3. Darwin , 1872 .
4. Scherer , 1979 , 1985 .
5. See , for example, a review by Murray and Arnott on human vocal emotion (1993) ,
which was recently brought t o our attention .
6. Rowell , 1962 .
7. Gaion i an d Evans, 1985, 1986a , 1986b.
8. Morto n an d Page, 1992 .
9. Lambrecht s an d Dhondt, 1986 .
10. I t may be that the conflict between th e ability to listen and the ability to concentrate
on talkin g is the foundatio n o f lie detectors. Th e person takin g a lie detector tes t may be
on the othe r en d o f a phone line , under no fea r o f direct attack . What is it that prevents a
liar's voice from soundin g like that of a truthful person ?
An inherent differenc e between a liar and one who is telling the truth is that the truthfu l
person ha s a true story that does not need t o be changed according to circumstance, while
a liar is making u p a story, an d his or her succes s depend s on the abilit y t o convinc e th e
listener of something that isn't true. The liar has to expend effor t t o make up the story. And
since the liar may not kno w in advance the listener's prior knowledg e o f the subject, he or
she needs to pay close attention to the listener's reaction in order to adapt the story, change
it slightlyand remember th e changesin order to be convincing. This close attention t o
the listener is very likely to affec t muscle s of the neck and head, and that in turn is likely to
affect th e voice to some degree. This differenc e ma y well be the one that lie detectors focu s
on (Streete r a t al, 1977) . I f the liar tries to rela x thes e muscles, hi s or her listening abilit y
will decrease and with it the abilit y to lie successfully .
11. Anava, 1992.
12. Katsir, 1985, 1991, 1995.
13. Zahavi, 1978b.
14. Payne, 1983.
15. Hultsc h and Todt, 1986 ; Todt an d Hultsch, 1995 .
16. Payne , 1983 .
17. McGregor , 1993 .
18. Pepperberg , 1991 ; Kaufman , 1991 .
19. Ofe r Hochberg, personal communication.
20. Ala n Kemp, personal communication .
21. Hultsc h and Todt, 1986 .
22. Loffred o an d Borgia, 1986 .
Notes 2 3
Chapter 7
1. Zu k e t al. , 1990 .
2. Holde r and Montgomerie, 1993 .
3. Darwin , 1871 .
4. Sutler , 1994 .
5. Evan s and Thomas, 1992 .
6. Evans , 1991 .
7. Andersson , 1982 .
8. Eibel-Eibelsfeldt , 1970 .
9. Se e also the discussio n o f fishes' fins in chapter 2 .
10. Ale x Kacelnic k pointe d ou t a logical weaknes s i n ou r argumen t that mane s an d
other feature s lesse n th e apparen t siz e o f bod y structures . Afte r all , w e asser t tha t erec t
feathers an d hair canno t b e mean t t o increase apparen t siz e since watchers ca n detect th e
deception. Ye t we ar e suggestin g an opposit e deceptionwhe n we claim that a frame o f
bristling hair or feathers is a handicap that reduces the apparent siz e of the animal. Should
watchers no t disregar d thi s deceptio n a s well , eve n i f i t i s base d o n a n optica l illusio n
(Ponzo's effectse e Fujit a e t al, , 1991) ? We accep t tha t th e watche r ma y know tha t th e
mane decreases the apparent size of the shape within it. But this effect makes it more difficult
for a slightly larger individual to show clearly its superiority in size, a superiority that would
have been obviou s i f it were no t fo r th e mane . This is a real handicap: onl y an individua l
who i s significantly larger than anothe r ca n afford a decoration tha t decrease s its apparent
size without impairin g its ability to show off that in fact i t is larger than others.
11. Richar d Wagner, personal communication .
12. Gior a Ilani , personal communication .
13. Se e also the discussio n o f human beards i n chapters 2 and 18 .
14. Darling , 1937 .
15. Glutton-Broc k et al. , 1982 .
16. Moller , 1991 .
Chapter 8
1. Hill , 1990 .
2. Endle r (1983 , 1987) , Lythgoe (1979), Hailman (1977) , Butcher and Rohwer (1989),
and other s suc h as Hamilton, WJ . (1973) , and Kingston (1933 ) have studied th e benefits
and drawback s of specific colors . To them it was a question o f balance between advertisin g
over distanc e o n th e on e han d an d mergin g with th e backgroun d t o avoi d enemie s an d
predators o n the other . They als o studied th e eye's sensitivity to various colors.
3. May r and Stresemann , 1950 .
4. Diamond , 1987 .
238 NOTE
5. Maier , 1993 .
6. Anderson , 1996 .
Chapter 9
1. Eisne r an d Meinwald , 1987, 1995 .
2. Schneider , 1992 .
3. Elli s et al, 1980 .
4. A t th e sam e time , though , hig h concentration s o f femal e pheromone impai r th e
ability of males to find females. In biologica l pes t control , syntheti c hormones ar e used t o
"confuse" males .
5. O n intoxicating beverages and the value of showing off the ability to imbibe without
getting drunk, see chapter 13 .
6. Naho n et al., 1995 .
7. Jackso n an d Hartwell, 1990a, 1990b .
8. Ulloa-Aguirre , 1995 .
9. Se e the bibliograph y in Nahon e t al. , 1995 .
10. Se e ibid.
11. Zahavi , 1993.
12. Snyde r and Bredt , 1992 .
13. Se e the bibliograph y in Nahon et al. , 1995 .
14. Zahavi , 1993.
Chapter 10
1. Zahavi , 1979.
2. Zahavi , 197Ib .
3. Morris , 1956 .
4. Se e chapter 12 .
5. Selander , 1972 .
6. Se e chapter 3.
7. Borgia , personal communication.
8. Osztreiher , 1992 .
9. Spiro , 1963 .
10. Va n Lawick-Goodall, 1970.
11. Rasa , 1986 .
Chapter 11
1. Trivers , 1974 .
2. Triver s further complicate d the problem by suggesting that according to kin selection,
the chil d also has some interest in its parents' reproduction becaus e of its genetic similarity
to its siblings; see Trivers, 1972 . Thi s complication is unnecessary, as we shall see when we
deal with the issue of kin selection in chapter 13 .
3. Zahavi , 1977a .
4. Heinroth , 1926 .
5. Feldma n an d Eshel, 1982 .
Notes 2 3
Chapter 12
1. Se e articles i n Hebrew by Pozis (1984) , Carmeli (1988) , Katsir (1991), Osztreiher
(1992), Anava (1992), Kalishov (1996), Perl (1996) , Zahavi, T. (1975) .
2. Late r in this chapte r we present graph s based o n some of the dat a that hav e bee n
collected s o far, much of which is as yet available only in Hebrew .
3. Osztreiher , 1996 .
4. Stache y and Koenig, 1990 ; Rowley and Russel, 1990 .
5. Va n Lawick-Goodall, 1971 .
6. Kruuk , 1972 .
7. Va n Lawick-Goodall, 1970 .
8. Rasa, 1986 .
9. Sherma n et al. , 1991 .
10. Bonner , 1967 .
11. Rosenberg , 1984 .
12. Se e Maynard Smith, 1964 , 1976b .
13. Hamilton , 1964 .
14. Trivers , 1971 .
15. Axelrod , 1986 .
16. Axelro d an d Hamilton, 1981 .
17. Ther e i s extensive literature o n these models. Se e a detailed discussio n an d bibli ography in Dawkins (1989) and a more up-to-date one in Sigmund (1993).
18. Stache y and Koenig , 1990 .
19. Se e chapter 1 , on prey-predator relations .
20. Zahavi , T., 1975 .
21. Carlisl e and Zahavi, 1986 .
22. Kalishov , 1996 .
23. Carlisl e and Zahavi, 1986 .
24. Kalishov , 1996 .
25. Carmeli , 1988 .
26. Slagsvold , 1984 , 1985 .
27. Carlisl e and Zahavi, 1986; Zahavi , 1989 .
28. Schjelderup-Ebbe , 1922 ; see Marler and Hamilton, 1966 .
29. Perl , 1996 .
30. Zahavi , 1988; Perl, 1996 .
31. Perl , 1996 .
32. Gaston , 1978 . Onl y one species o f babblers i n India lives in pairs .
33. Komdeur , 1992 , 1994 .
34. Woolfende n an d Fitzpatrick , 1984, 1990 .
35. Kofor d et al., 1990 .
36. Faabor g an d Bednarz, 1990 .
37. Se e Alexander, 1987 ; De Waal, 1996 .
24O NOTE
Chapter 13
1. Se e a detailed discussio n in Cronin, 1991 .
2. Alexander , 1974 .
3. Se e chapter 14 .
4. Wilson , 1971 .
5. West-Eberhard , in her stud y o f Polistes canadensis (1986) , showed that when on e
queen clearl y controls the others, the level of aggression in the nest is low, while when there
are only slight differences betwee n th e queens, aggression is high and there may be life-anddeath struggle s among the partners.
6. West , 1969 ; West-Eberhard, 1984 ; Gadagkar, 1991 ; Ito , 1993 .
7. The was p Vespula germanica was brought by European s to Australia . In tropica l
regions, i t turne d ou t tha t it s colonie s coul d surviv e the winter , an d ne w colonies o f this
species in such regions are formed by coalitions of several queens. Se e Ito, 1993 .
8. Wilson , 1971 ; Heinze e t al. , 1994 .
9. Trivers , 1985 .
10. I t ma y be tha t some workers d o indeed avoi d working, but thi s doe s no t deman d
any special explanation. It i s the fact that workers do invest in the colony, as indeed most
do, that demands explanation .
11. West , 1969 .
12. Gadagkar , 1991; Heinze et al., 1994 .
13. Marle r an d Hamilto n (1966 ) defin e pheromone s a s chemicals secreted b y one individual in order to elicit a specific reaction i n another individual of the same species. As a
rule, pheromone s ar e mixture s o f chemicals, an d i n mos t case s their specifi c component s
are not known . Thus , we use the term s queen pheromone or pheromones without gettin g
into the specific s of one material or another .
14. Isha y et al. (1967, 1968 ) found that worker orienta l hornets cannot make sugars out
of proteins, a process known as gluconeogenesis; they feed the larvae proteins, and eat sugars
they get from th e larvae. If such mutual feeding is found between th e larvae and the adul t
workers of other socia l insects, it will provide another reasonprobably the main onefor
workers to feed the larvae and take care of them. However, thi s very interesting area requires
more research.
15. Winsto n an d Slessor , 1992.
16. Engel s and Imperatriz-Fonseca, 1990 .
17. Va n der Blom, 1986 .
18. Rosele r an d Honk , 1989 ; se e also Velthuis, 1990 .
19. Diamond , 1990 , 1992 .
20. Veblen , 1899 .
21. Trivers , 1974 , 1985 . Not e tha t by this definition, a host taking care of its parasite's
offspring i s an altruist, and indeed Triver s s o defines it (1985). By the same definition, when
a helper i s sterile t o begin with , it s reproduction canno t diminis h an y further and thus its
help canno t be see n as altruism.
22. Trivers , 1971 .
23. Hamilton , 1964 .
Notes 2 4
Chapter 14
1. Trivers , 1972 , discussed i n detail the implications of the conflic t of interest between
the genders, an d many have studied th e subject since. We ar e not attemptin g to challeng e
his treatment o f the subject but rathe r to add some observations fro m ou r own perspective .
2. Selander , 1965 , 1972 ; Orians, 1969 ; Emle n and Oring, 1977 .
3. Gustafson , 1989 ; Beissinger , 1986; Beissinge r and Snyder , 1987.
242 NOTE
Chapter 15
1. Thi s descriptio n is based o n Bonner (1991 ) an d Nanjundia h an d Sara n (1992).
2. Se e Atzmony et al., 1997.
3. cAM P is a chemical with many roles in all living organismsfrom bacteria to mammals, including humans . It i s considered a secondary messenger transferring stimuli fro m
the cell membrane t o the inside of the cell.
4. Shaulsk i and Loomis (1993) found that some of the amebas that ended up as spores
showed sign s of having been prestalk before that. In other words, at the end of the process
of migration and stal k formation, some of the prestalk ameba s manage to become spores .
5. Se e Atzmony et al., 1997 .
6. Bruc e Levin, personal communication .
7. Atzmon y and Nanjundiah, personal communication .
8. Se e Rosenberg, 1984 .
9. Se e Zahavi and Rait, 1984 .
10. Shaulsk i and Loomis, 1995 .
Chapter 16
1. Dawkin s and Krebs , 1979 ; Rothstein, 1990 .
2. Davie s and Brook, 1989 .
3. Lotemetal , 1991 , 1995 .
4. Lote m wrote another article about th e dangers o f evolving the abilit y to recogniz e
a parasite's nestling and deser t it or throw it out of the nest. See Lotem, 1993b .
Notes 2 4
5. Researc h done b y Yoram Shpirer , Amot z Zahavi, Arnon Lotem , an d Stev e Rothstein.
6. Sole r et al. , 1995 .
7. Zahavi , 1979.
8. Se e chapters 3, 12 , and 14.
9. Newton , 1989b ; Scott, 1988 ; Owen an d Black, 1989 .
10. Yom-Tov , 1989 .
11. Ingle , 1911 ; Wyllie, 1975 ; Witherby et al. , 1949 .
12. Zahavi , 1979.
13. Sole r et al. , 1995 .
14. J . Tengo , University of Uppsala, Sweden, personal communication .
15. Tengo , 1984 .
16. M . Sorensen, personal communication.
17. Smit h et al. , 1984 .
18. Oberski , 1975 ; Kuris , 1974.
19. Schwammberger , 1993 .
20. Salyer s and Whitt, 1994.
Chapter 17
1. Zahavi , 197la.
2. Ward , 1965 .
3. Darling , 1938 .
4. Unfortunately , Ward, th e partne r with who m Amot z developed th e ide a o f information centers , died a t an early age.
5. War d and Zahavi, 1973 .
6. Parker-Rabenold , 1978 ; Broo m et al., 1976 ; Heinrich, 1988 .
7. Brown , 1986 .
8. Heinrich , 1988 .
9. Wagner , 1996 .
10. Zahavi , 1983, 1995 .
11. Ward , 1972 .
12. Fear e e t al. , 1974 .
13. Heredi a e t al. , 1991 ; Hiraldo et al., 1993 .
14. Bucher , 1992.
15. Wynne-Edwards , 1962 .
16. Marx , personal communication.
17. Veblen , 1899 .
18. Ibid .
19. Se e Wynne-Edwards, 1962 .
20. I n ou r origina l articl e on informatio n center s (War d and Zahavi , 1973 ) w e mad e
something o f a group-selectio n argumen t ourselves . W e hav e sinc e recognize d tha t early
error an d have suggested tha t othe r explanation s shoul d b e sought for the communal displays at roosts (Zahavi , 1985b) . Thi s subjec t has received further treatmen t in our respons e
to a n article by Richner and Heeb (Zahavi, 1996).
21. Zahavi , 1983, 1995 .
22. Se e chapter 1 .
244 NOTE
Chapter 18
1. Shepher , 1983 .
2. Hess , 1965 .
3. Eibel-Eibelsfeldt , 1971 .
4. Se e chapter 8.
5. 2 Samuel 20:9.
6. Se e chapter 7.
7. Morris , 1967 .
8. Car o and Seller, 1990 .
9. Seve r and Mendelsohn, 1989 .
10. D e Waal , 1995 .
11. Strahl , 1988 .
12. Se e chapter 10.
13. Zahavi , 1971b.
14. Trivers , 1985 .
15. Wagner , 1996 .
16. Se e chapter 11 .
17. Th e gra y parrot Alex; see Pepperberg, 1991 .
18. Th e exception is among the most highly social bees, wasps, ants, and termites, whose
communities include thousands of individuals.
19. Th e differences between a language of nonverbal vocalizations and a verbal language
is like the differenc e betwee n a n analog speedometer an d a digital speedometer. An analog
speedometer's needl e let s us estimate speed prett y precisely, even if there are only two or
three numbers o n the face of the speedometer. A digital speedometer, which displays numbers, i s limited t o th e precisio n o f these numbers . I f th e digit s chang e with onl y every 5
additional mile s per hour , the digita l speedomete r wil l not sho w the differenc e between ,
say, 1 1 mph an d 1 4 mphwhile an analog speedometer will .
20. Zahavi , 1980 .
21. Frit h and Frith, 1990 ; Diamond, 1991 .
22. Se e chapter 4.
23. Benedict , 1946 .
24. Bakal , 1979 .
25. Veblen , 1899 .
BIBLIOGRAPHY
246 BIBLIOGRAPH
Bibliography 2 4
248 BIBLIOGRAPH
. 1995 . Th e chemistr y of sexual selection. Proc. Natl. Acad. Set. US A 92: 50-55.
Ellis, P.E., L.C . Brimacombe, LJ. McVeigh, and A. Dignan. 1980. Laboratory experiments
on th e disruptio n o f matin g in th e Egyptia n cotto n leafwor m Spodoptera littoralis
(Lepidoptera: Noctuidae ) b y excesse s o f femal e pheromones . Bull. Ent. Res. 70 :
673-84.
Emlen, S.T., N.J. Demong, an d DJ. Emlen. 1989. Experimenta l induction of infanticide in
female wattled jacanas. Auk 106 : 1-7 .
Emlen, S.T., and L.W . Oring. 1977 . Ecology, sexual selection an d the evolution of mating
systems. Science 197 : 215-23.
Endler, J.A. 1983. Natural and sexual selection of color patterns in Poeciliid fishes. Environ.
Biol. o f Fishes 9: 173-90.
. 1987 . Predation , light intensity, and courtshi p behaviour in Poecilia reticulata (Pisces: Poeciliidae). Anim. Behav. 35: 1376-85.
Engels, W., and V.L. Imperatriz-Fonseca. 1990. Caste development, reproductive strategies
and control of fertility in honey bees and stingless bees. In Social insects: An evolutionary
approach t o caste and reproduction, ed . W. Engels , 167-230. Berlin: Springer-Verlag.
Eshel, I, 1978a. A critical defence of the handicap principle. /. Theor. Biol. 70: 245-50.
. 1978b . O n a prey-predator nonzero-su m game an d th e evolutio n o f gregarious
behavior o f evasive prey. Amer. Nat. 112 : 787-95.
Eshel, I., and U. Metro. 1988 . Th e three brothers' problemkin selection with more than
one potential helper . I: The case of immediate help. Amer. Nat. 132 : 550-66.
Evans, C.S. 1985 . Displa y vigour and subsequent fight performance i n the Siamese fighting
fish Betta splendens. Behavioural Processes 11: 113-21.
Evans, M.R. 1991. The siz e of adornments of male scarlet-tufted malachite sunbirds varies
with environmenta l conditions, a s predicted b y handicap theories . Anim. Behav. 42:
797-803.
Evans, M.R., and A.L.R . Thomas. 1992 . The aerodynami c and mechanica l effects o f elongated tails in the scarlet-tufted malachite sunbird: the cost of a handicap. Anim. Behav.
43: 337-47.
Ewer, R.F. 1968 . Ethology o f mammals. London: Logo s Press .
Faaborg, J., an d J.C. Bednarz . 1990 . Galapago s an d Harris ' hawks : Divergent cause s of
sociality in tw o raptors . I n Cooperative breeding i n birds, ed . P.B . Stace y and W.D .
Koenig, 357-84. New York: Cambridge University Press.
Feare, C.J., G.M. Dunnet , and LJ. Patterson. 1974 . Ecological studie s of the rook (Corvus
frugilegus L. ) in north-east Scotland ; foo d intake an d feeding behavior . /. Appl. Ecol.
11: 867-896.
Feldman, M.W., and I. Eshel. 1982 . On the theory of parent-offspring conflict : A two-locus
genetic model. Amer. Nat. 119 : 285-92.
Fisher, R.A. 1930 . Th e genetical theory o f natural selection. London: Clarendo n Press .
Fishman, L . 1977 . Wheatearsliv e warnin g system s agains t snake s (i n Hebrew) , leva
Va'aretz 19 : 198 .
FitzGibbon, C.D. , an d J.H. Fanshawe . 1988 . Slottin g in Thompson's gazelle : An hones t
signal of condition. Behav. Ecol. Sociohiol. 23: 69-74.
Forslund, P . 1990 . Mat e chang e reduces reproductio n i n th e barnacl e goose (Branta leucopsis)the advantag e of having an old partner. Acta XX Con. Inter. Ornithol. 470.
Bibliography 2 4
Foster, M.S . 1981. Cooperativ e behavior an d social organization in the swallow-tailed manakin (Chiroxiphia caudata). Behav. Ecol. Sociobiol. 9: 167-77.
Frith, C.B. , and D.W . Frith . 1990 . Archbold' s bowerbird , Archboldia papuensis (Ptilono rhynchidae), uses plumes from king bird o f paradise, Pteridophora alberti (Paradisaeidae), as bower decoration . Em u 90 : 136-37.
Fugle, G.N., S.I . Rothstein, C.W. Osenberg, an d M.A. McFinley. 1984 . Signal s of status in
wintering white-crowne d sparrow s (Zonotrichia leucoptrys gambeli). Anim. Behav. 32:
86-93.
Fujita, K. , D.S . Blough , an d P.M . Blough . 1991 . Pigeon s se e the Ponz o illusion . Anim.
Learning Behav. 19:283-93.
Gadagkar, R. 1991. Belonogaster, Mischocyttarus, Parapolybia, an d independent-founding
Ropalidia. In The social biology o f wasps, ed . K.G. Ross and R.W. Matthews, 149-200.
Ithaca, NY : Cornell University Press.
Gadagkar, R., and N.V . Joshi. 1985 . Colon y fission in a social wasp. Current Sci. 54:57-62.
Gaioni, S.J. , an d C.S . Evans . 1985 . Th e rol e o f frequenc y modulation i n controllin g th e
response of mallard ducklings (Anas platyrhynchos) to conspecific distress calls. Anim.
Behav. 33: 188-200.
. 1986a . Mallard ducklin g respons e to distres s calls with reduced variability: Con straint on stereotypy in a "fixed actio n pattern." Ethology 72: 1-14 .
1986b. Perception o f distress call s i n mallard duckling s (Anas platyrhynchos). Be haviour 99: 250-74.
Gaston, AJ . 1977 . Socia l behaviour withi n groups o f jungle babblers (Turdoides striatus).
Anim. Behav. 25: 828^8.
. 1978. The evolution o f group territorial behaviour and cooperative breeding. Amer.
Nat. 112 : 1091-1100 .
Gibbs, H.L., an d P.R. Grant . 1987 . Oscillatin g selectio n o n Darwin's finches. Nature 327:
511-13.
Gibson, R.M. , J.W. Bradbury , an d S.L . Vehrencamp. 1991 . Mat e choic e i n lekking sag e
grouse revisited : Th e role s o f vocal display , femal e site fidelit y an d copying . Behav.
Ecol. 2: 165-80.
Gibson, R.M., and J. Hoglund . 1992 . Copyin g and sexual selection. Tree 7: 229-32.
Goldstein, H. , D . Eisikovitz, and Y. Yom-Tov. 1986 . Infanticid e in the Palestine sunbird s
Nectarina osea. Condor 88 : 528-29.
Grafen, A . 1990a. Biologica l signals as handicaps. / . Theor. Biol. 144 : 517-46.
. 1990b . Sexua l selection unhandicappe d b y the Fisher process . /. Theor. Biol. 144:
473-516.
Greenewalt, C.H. 1986 . Bird song: Acoustics and physiology. Washington , DC: Smithsonian
Institution Press .
Gustafsson, L . 1989 . Collare d flycatcher. In Lifetime reproduction i n birds, ed . I. Newton ,
75-88. London: Academi c Press.
Hailman, J.P. 1977 . Optical signals: Animal communication and light. Bloomington, IN :
Indiana Universit y Press.
Haldane, J.B.S. 1932. Th e Causes of Evolution. London: Longmans Green. Reprint. Princeton: Princeton Scienc e Library, 1990.
. 1955 . Populatio n genetics . New Biology 18 : 34-51.
25O BIBLIOGRAPH
Hamilton, W.D. 1964 . The genetical evolution of social behaviour. /. Theor. Biol 1: 1-52 .
Hamilton, W.D. , an d M . Zuk . 1982 . Heritabl e tru e fitnes s an d brigh t birds : A rol e fo r
parasites? Science 218: 384-87.
Hamilton, WJ. III. 1973 . Life's color code. New York: McGraw-Hill .
Hunter, C.P. , an d P.D. Dwyer . The value of objects to satin bowerbirds (Ptilonorhynchu s
violaceus). Emu (i n press).
Hasson, O . 1991a . Pursuit-deterren t signals : Communication between pre y and predator .
Tree 6: 325-29.
. 1991b. Sexual displays as amplifiers: Practical examples with an emphasis on feather
decorations. Behav. Ecol. 2: 189-97.
Hasson, O. , R . Hibbard, an d G . Cebballos . 1989 . Th e pursuit-deterren t function of tail
wagging in the zebra-taile d lizard (Callisaurus draconoides). Canad. ]. Zoo/. 67: 1203 09.
Heinrich, B. 1988 . Winte r foragin g at carcasse s by the thre e sympatri c corvids, with emphasis on recruitment by the raven , Corvus corax. Behav. Ecol. Sociobiol. 23: 141-56.
Heinroth, O.J., an d M. Heinroth. 1926. Die Voget Mitteleuropas. Berlin-Lichterfelde : Hugo
Bermuhler-Verlag.
Heinze, J., B . Holldobler, and C . Peeters. 1994 . Conflic t an d cooperatio n i n ant societies.
Naturwissenschaften 81 : 489-97.
Hendry, L.B., E.D. Bransome, M.S. Hutson, and L.K. Campbell. 1984 . A newly discovered
stereochemical logic in the structure of DNA suggests that the genetic code is inevitable.
Perspectives i n Biology an d Medicine 27 : 623-51.
Hendry, L.B., and V.B. Mahesh. 1995 . A putative step i n steroid hormone action involves
insertion o f steroi d ligand s int o DN A facilitate d b y recepto r proteins . / . Steroid
Biochem. Molec. Biol. 55: 173-83.
Heredia, B. , J.C. Alonso , and F. Hiraldo. 1991 . Spac e and habitat use by red kites, Milvus
milvus, durin g winte r i n th e Guadalquivi r marshes : A comparison betwee n residen t
and wintering populations. Ibis 133: 374-81.
Hess, H.E. 1965 . Attitud e and pupil size. Set. Amer. 212: 46-54.
Hill, G.E. 1990 . Female house finches prefer colorful mates: Sexual selection for a conditiondependent trait . Anim. Behav. 40: 563-72.
Kingston, R.W.G. 1933 . Th e meaning of animal colour and adornment. London: Arnold.
Hiraldo, F. , B. Heredia, an d J.C. Alonso . 1993 . Communal roosting of wintering red kites,
Milvus milvus (Aves, Accipitridae): Social feeding strategies for the exploitation of food
resources. Ethology 93 : 117-24.
Hoglund, J., R. Montgomerie, and F. Widemo. 1993 . Costs and consequences of variation
in the siz e of ruff leks . Behav. Ecol. Sociobiol. 32: 31-39.
Hogan-Warburg, A J. 1966. Social behavior of the ruff, Philomachus pugnax (L). Ardea 54:
109-229.
Holder, K. and R. Montgomerie. 1993. Context and consequences of comb displays by male
rock ptarmigan. Anim. Behav. 45: 457-70.
Holldobler, B. , and E.O. Wilson . 1990 . Th e ants. Cambridge: Harvard Universit y Press.
Hultsch, H. , an d D . Todt . 1986 . Signa l matching: Zeichenbildun g durc h mustergleiche s
Antworten. Semiotik 8 : 233-44.
Huxley, J.S. 1914 . The courtshi p habits of the great crested grebe (Podiceps cristatus) with
an addition to the theory of sexual selection. Proc. Zool. Soc. London 35: 491-562.
Bibliography 2 5
252 BIBLIOGRAPH
Bibliography 2 5
McGregor, P.K . 1993 . Signalling in territorial systems : A context fo r individual identifica tion, ranging and eavesdropping. Phil. Trans. R. Soc. Land. B 340: 237-44.
McKaye, K.R. 1991. Sexua l selection an d the evolution of the cichlid fishes of Lake Malawi.
In Cichlid fishes ' behaviour, ecology an d evolution, ed. M.H.A . Keenleyside , 241-57.
London: Chapma n and Hall.
Mock, D.W. 1984 . Siblicidal aggression and resource monopolization in birds. Science 225:
731-33.
Moller, A.P . 1990a . Fluctuatin g asymmetr y in mal e sexual ornaments may reliably reveal
male quality. Anim. Behav. 40: 1185-87.
. 1990b . Mal e tail length an d femal e mate choice in the monogamous swallow, Hirundo rustica. Anim. Behav. 39: 458-65.
. 1990c . Sexua l behavior is related to badge size in the house sparrow Passer domesticus. Behav. Ecol. Sociobiol. 27: 23-29.
. 1991. Influence of wing and morphology on the duration of song flights in skylarks.
Behav. Ecol. Sociobiol. 28: 309-14.
. 1992 . Femal e swallow preferences for symmetrical male sexual ornaments. Nature
357: 238-240.
. 1994 . Sexual selection and the barn-swallow. Oxford: Oxford University Press.
Montgomerie, R . (convenor) . 1986 . Symposiu m on mat e guarding . Acta XIX Con. Inter.
Ornithol. 408-53. Ottawa .
Moore, AJ. 1988. Female preferences, male social status, and sexual selection in Nauphoeta
cinerea. Anim. Behav. 36: 303-5.
Moreno,}., M. Soler, A.P. Moller, an d M . Linder. 1994 . The function of stone carrying in
the black wheatear (Oenanthe leucora). Animal Behav. 47: 1297-1309.
Morris, D. 1956 . Th e function an d causatio n of courtship ceremonies . In L'instinct dans le
comportement des animaux et de I'homme, ed. P.P. Grasse , 261-86. Fondation SingerPolignae. Paris: Masson.
. 1957 . "Typica l intensity " an d it s relationship t o th e proble m o f ritualization. Behaviour 11: 1-12 .
. 1967 . The naked ape. Ne w York: McGraw-Hill .
. 1990 . Animalwatching. New York: Crown.
Morton, E.S . 1977 . O n th e occurrenc e an d significanc e of motivation-structural rule s in
some birds an d mammal sound. Amer. Nat. Ill: 855-69.
Morton, E.S. , L. Forman, and M. Braun. 1990. Extrapai r fertilizations and the evolution of
colonial breeding in purple martins. Auk 107 : 275-83.
Morton, E.S. , and J. Page. 1992 . Animal talk. New York: Random House.
Motro, U. , and I. Eshel. 1988 . Th e three brothers' problem : Ki n selection wit h more than
one potential helper. II: The case of delayed help. Amer. Nat. 132 : 567-75.
Munehara, H., A. Takenaka, and O. Takenaka. 1994. Alloparental care in the marine sculpin
(Alcichthys alcicornis, Pisces: Cottidae): Copulating in conjunction with parental care.
/. Ethol. 12: 115-20.
Murray, I.R., and J.L. Arnott. 1993. Towards the simulation of emotion in synthetic speech:
A revie w o f th e literatur e o n huma n voca l emotion . / . Acoust. Soc. Am. 92 : 1097 1108.
Nahon, E., D. Atzmony, A. Zahavi, and D. Granot. 1995 . Mate selection i n yeast: A reconsideration o f the signal s and the message encoded b y them. /. Theor. Biol. 172 : 31522.
254 BIBLIOGRAPH
Bibliography 2 5
Redondo, T., and F. Castro. 1992 . Signalling of nutritional need by magpie nestlings. Ethology 92 : 193-204.
Reyer, H.U . 1990 . Pie d kingfishers : ecological cause s an d reproductiv e consequence s of
cooperative breeding . In Cooperative Breeding in Birds, ed . P.B. Stacey and W.D. Koenig, pp. 527-559. Cambridge, UK: Cambridge Universit y Press.
Rhisiart, A.P. 1989 . Communicatio n an d antipredator behaviour. D.Phil, thesis, University
of Oxford .
Ridley, M. 1981 . Ho w the peacoc k go t his tail. New Sci. 91: 398-401.
Ritland, D.B . 1991a . Unpalatabilit y o f vicero y butterflie s (Limenitis archippus) an d
their purporte d mimicr y models , Florid a queen s (Danaus gilippus). Oecologia 88 :
102-8.
. 1991b . Revising a classic butterfly mimicry scenario: Demonstration o f Muellerian
mimicry between Florida viceroys (Limenitis archippus floridensis) and queens (Danaus
gilippus berenice). Evolution 45: 918-34.
Rohwer, S., and P.W. Ewald. 1981. Th e cos t of dominance and advantage of subordination
in a badge signalin g system. Evolution 35: 441-54.
Rohwer, S. , an d F.C . Rohwer . 1987 . Statu s signallin g in Harris ' sparrows : Experimenta l
deceptions achieved. Anim. Behav. 26: 1012-22.
Roper, T. 1986 . Badge s of status in avian societies. Ne w Sci. 109: 38^(0.
Roseler, P.F. , an d C.GJ . Honk . 1989 . Caste an d reproductio n i n bumblebees. I n Social
insects: An evolutionary approach t o caste an d reproduction, ed . W . Engels, 147-166 .
Berlin: Springer-Verlag.
Rosenberg, E . 1984 . Myxobacteria. Ne w York: Springer-Verlag.
Rothstein, S.I . 1990 . A model syste m for coevolution : avia n brood parasitism . Ann. Rev.
Ecol. Syst. 21 : 481-508.
Rowel, T.E . 1962 . Agonisti c noise s o f th e rhesu s monke y (Macaca mulata). Proc. R . Soc.
London 138 : 91-96.
Rowley, I., and E . Russel. 1989 . Splendi d fairy-wren . In Lifetime reproduction i n birds, ed .
I. Newton, 233-52. London: Academic Press.
. 1990 . Splendi d fairy-wren : Demonstrating th e importanc e o f longevity. In Cooperative breeding i n birds, ed . P.B . Stace y and W.D . Koenig , 1-30 . Cambridge , UK :
Cambridge University Press .
Ryan, MJ. 1990 . Sexua l selection sensor y systems, and sensor y exploitation. Oxford Surv.
Evol. Biol. 7: 157-95.
Ryan, MJ., M.D. Tuttle , an d A.S . Rand. 1982 . Bat predation an d sexual advertisement in
a neo-tropical anuran. Amer. Nat. 119 : 13639 .
Sade, D.S. 1972 . A longitudinal stud y of social behavior o f Rhesus monkeys. In The functional an d evolutionary biology o f primates, ed. R . Tuttle , 378-98 . Chicago : Aldine Atherton.
Saino, N., A.P. Moller, and A.M. Bolzern. 1995 . Testosterone effect s on the immune system
and parasit e infestations in the bar n swallo w (Hirundo rustica): A n experimental tes t
of the immunocompetenc e hypothesis . Behav. Ecol. 6: 397-404.
Salyers, A.A. , and D.D . Whit . 1994 . Bacterial pathogenesis. Washington, DC : American
Society for Microbiology .
Scherer, R.K . 1979 . Nonlinguisti c voca l indicator s o f emotio n an d psychopathology . I n
Emotions in personality an d psychopathology, ed . C.E. Izard, 493-525. New York: Plenum.
256 BIBLIOGRAPH
Bibliography 257
Snyder, H.S., an d D.S. Bredt. 1992 . Biological roles of nitric oxide. Set. Am. 266 : 58-67.
Soler, M.,J. Soler, J.G. Martinez , and A.P. Moller. 1995. Magpie host manipulation by great
spotted cuckoos : Evidence fo r a n avian mafia? Evolution 49: 770-75.
Sordahl, T.A . 1990 . Th e risk s o f avia n mobbin g an d distractio n behavior : A n anecdota l
review. Wilson Bull. 102 : 349-352.
Spiro, M.E . 1963 . Kibbutz, adventure in Utopia. Ne w York: Schocken Books .
Stacey, P.B. , an d W.D . Koenig. 1990 . Cooperative breeding in birds: Long-term studies of
ecology an d behaviour. Cambridge, UK: Cambridge Universit y Press.
Strahl, S.D . 1988 . Th e social organization and behaviour of the hoatzin, Opisthocomus hoatzin, in central Venezuela. Ibis 130 : 483-501.
Streeter, L.A., R.M. Krauss, V. Geller, C . Olson, and W. Apple. 1977 . Pitch chang e during
attempted deception. /. o f Personality an d Soc. Psychol. 35: 345-50.
Sugiyama, Y. 1967. Socia l organisation of hanuman langurs. In Social communication among
primates, ed. S.A . Altman. Chicago: University of Chicago Press .
Sutler, E. 1994 . Ar e the peacock' s trai n feather s really upper tai l coverts? /. fur Ornithol.
135: 57 .
Taborsky, M. 1994. Parasitism and alternative reproductive strategie s in fish. Adv. i n Behav.
Studies 28: 1-100.
Tengo, J . 1984 . Territoria l behaviou r o f th e kleptoparasit e reduce s parasiti c pressur e i n
communally nesting bees. Abstract volume: XVII International Congress of Entomology
510.
Thornhill, R. 199 2 a. Female preference fo r th e pheromon e of males wit h lo w fluctuatin g
asymmetry in th e Japanese scorpionfl y (Panorpa japonica, Mecoptera) . Behav. Ecol. 3:
277-83.
. 1992b. Fluctuating asymmetry, interspecific aggressio n an d male mating tactic s in
two species of Japanese scorpionflies . Behav. Ecol. Sotiobiol. 30: 357-63.
Thornhill, R. , and J. Alcock. 1983. The evolution of insect mating systems. Cambridge, MA:
Harvard Universit y Press.
Tinbergen, N . 1953 . The herring gull's world. London: Collins .
. 1965. Some recent studies of the evolution o f sexual behavior. In Sex and behavior,
ed. F.A. Beach, 1-33 . Ne w York: Wiley.
Todt, D. , and H. Hultsch. 1995 . Acquisitio n and performance of song repertoires: Ways of
coping with diversity and versatility. In Ecology and evolution of acoustic communication
in birds, ed . D. Kroodsma and E. Miller. Ithaca , NY: Cornell University Press .
Trivers, R. 1971. Th e evolutio n o f reciprocal altruism . Quart. Rev. Biol. 46: 35-57.
. 1974 . Parent-offspring conflict. Amer. Zoo/. 14 : 249-64.
. 1985. Social evolution. Menlo Park, CA: Benjamin/Gumming Publication Company.
Trivers, R.L . 1972 . Parenta l investmen t an d sexua l selection . In Sexual selection and the
descent o f man 1871-1971, ed . B. Campbell, 136-179 . London: Heinemann .
Ulloa-Aguirre, A. , A.R . Midgle y Jr., I.Z . Beitins , an d V . Padmanabhan . 1995 . Follicle stimulating isohormones : characterizatio n an d physiological relevance . Endochrine Reviews 16 : 765-787.
Van de r Blom , J. 1986 . Reproductiv e dominanc e within colonie s o f Bombus terrestris. Behaviour 97: 37-49.
Van Lawick , H., andj. Va n Lawick-Goodall. 1970 . Innocent killers. London: Collins .
Van Lawick-Goodall , J. 1971 . In th e shadow of man. London: Collins .
258 BIBLIOGRAPH
Van Rhijn, J.G. 1973 . Behavioura l dimorphism i n male ruffs (Philomachus pugnax L.). Behaviour 47: 153-229.
Veblen, T . 1899 . Th e theory o f th e leisure class. New ed., ed. C.W. Mills. New Brunswick,
NJ: Transaction Publishers , 1992 .
Velthuis, H.W. 1990. Chemica l signal s and dominance communication in the honeybee Apis
mellifera (Hymenoptera : Apidae). Entomol. Gener. 15(2): 83-90.
Wagner, R . 1992. Extra-pair copulations i n a lek: The secondar y mating system of monogamous razorbills. Behav. Ecol. Sotiobiol. 31: 63-71.
Wagner, R. , M.D . Schug , and E . Morton . 1996 . Confidenc e in paternity , actual paternity
and paternal effort b y purple martins. Anim. Behav., in press.
Wagner, R . H., 1996 . Wh y d o female birds rejec t copulation s fro m thei r mates? Ethology
102: 465-480.
Wallace, A.R . 1889 . Darwinism: An exposition of th e theory o f natural selection with some
of it s applications. London : Macmillan .
Ward, P. 1965 . Feedin g ecolog y of the black-face d dioch (Quelea quelea) i n Nigeria. Ibis
107: 173-214.
. 1972 . The functiona l significance of mass drinking flight s by sandgrouse (Pteroclididae). 7te 114 : 533-36.
Ward, P. , an d A. Zahavi. 1973 . Th e importance of certain assemblages o f birds as "infor mation-centers" fo r food-finding. Ibis115: 517-34.
Watson, J.P., an d R . Thornhill. 1994 . Fluctuatin g asymmetr y and sexua l selection. Tree 9:
21-25.
Weiner, J. 1994 . Th e beak of th e finch. New York: Vintage.
West, M.J. 1969 . Th e socia l biology of polistine wasps. Univ. Mich. Mus. Zoo/. Misc. Publ.
140: 1-101.
West-Eberhard, M.J. 1975 . Th e evolutio n of social behavior by kin selection. Quar. Rev.
Biol. 50: 1-33 .
. 1984 . Sexua l selection, competitiv e communicatio n an d species-specifi c signals in
insects. In Insect communication, ed. T. Lewis, 283-324. New York: Academic Press.
. 1986 . Dominanc e relations i n Polistes canadensis (L.) , a tropical socia l wasp. Monitore Zoo/. Ital. (N.S. ) 20: 263-81.
Wiklund, C., and T. Jarvi. 1982. Survival of distasteful insects afte r bein g attacked by naive
birds: A reappraisal of the theory of aposematic coloration evolving through individua l
selection. Evolution 36: 998-1002.
Wilhelm, K. V., H. Comtesse , and W. Pfiumm. 1980 . Zu r Abhangigkeit des Gesangs vom
Nahrungsangebot beim Gelbbauchnektarvogel (Nectarinia venusta.)Z, Tierpsychol. 54 :
185-202.
. 1982 . Influenc e of sucros e solutio n concentratio n o n th e son g and courtshi p be haviour of the male yellow-bellied sunbir d (Nectarinia venusta). Z. Tierpsychol. 60:27 40.
Williams, G.C. 1966 . Adaptation and natural selection: A critique of some current evolutionary thought. Princeton: Princeto n Universit y Press.
. 1994. Natural selection: Domains, levels and challenges. Oxford: Oxford University
Press.
Willson, D.S. , an d E . Sober . 1994 . Reintroducin g grou p selectio n t o huma n behaviora l
sciences, behavioral and ^>rain Sciences, 17 : 585-654.
Bibliography 2 5
Wilson, E.O . 1971. The insect societies. Cambridge: Harvard Universit y Press.
. 1975 . Sociobiology: The ne w synthesis. Cambridge, MA : Belknap Press .
Winston, M.L. , and K.N . Slessor. 1992 . The essenc e o f royalty: Honey be e quee n phero mone. Amer. Set. 80: 374-85.
Witherby, H.F., F.C.R. Jourdain, N.F. Ticehurst, and B.W. Tucker. 1943 . The handbook of
British birds. London : Witherby.
Woolfenden, G.E. , and J.W. Fitzpatrick. 1984 . The Florida scrub jay. Princeton: Princeto n
University Press.
. 1990. Florida scrub jays: A synopsis after 1 8 years of study. In Cooperative Breeding
in Birds, ed . P.B. Stacey and W.D. Koenig, 239-66. Cambridge: Cambridge University
Press.
Wyllie, I. 1975 . Study of cuckoos and ree d warblers. Br. Birds 68 : 369-78.
Wynne-Edwards, V.C. 1962. Animal dispersion i n relation to social behaviour. Edinburgh:
Oliver an d Boyd.
. 1986 . Evolution through group selection. Oxford: Blackwell Scientific Publicatio ns.
Yom-Tov, Y. 1989 . Seemingly maladaptive behaviours, individua l recognitio n an d hierarchy. Ornis Scand. 20: 2.
Zahavi, A . 1971a . Th e functio n o f pre-roos t gathering s an d communa l roosts . Ibis 113:
106-09.
. 1971b . Th e socia l behavior of the white wagtail, Motacilla alba, wintering in Israel.
Ibis 113 : 203-11.
. 1974 . Communal nestin g by th e Arabia n babbler , a cas e o f individual selection .
Ibis 116 : 84-87.
. 1975 . Mate selection: A selection for a handicap. /. Theor. Biol. 53: 205-14.
. 1976. Cooperative nestin g in Eurasian birds. I n Acta XVI Con. Inter. Ornithol., ed.
HJ. Frith, an d J.H. Calaby, 685-93. Canberra , Australia.
. 1977a . Reliability in communication system s and th e evolutio n o f altruism. In Evolutionary ecology, ed . B . Stonehouse an d C.M . Perrins, 253-59. London : Macmillan
Press.
. 1977b . The cos t o f honesty (furthe r remark s on the handica p principle). ], Theor.
Biol. 67: 603-5.
. 1977c . Th e testin g of a bond. Anim. Behav. 25: 246-47.
. 1978a . Decorative pattern s an d th e evolutio n of art. New Sci. 80: 182-84.
. 1978b . Wh y shouting. Amer. Nat. 113: 155-56.
. 1979 . Parasitism and nes t predation i n parasitic cuckoos. Amer. Nat. 113: 157-59.
. 1980 . Ritualization and th e evolutio n of movement signals . Behaviour 72: 77-81.
. 1981a . Natura l selection, sexua l selection an d the selection o f signals. In Evolution
today, ed . G.G.E. Scudder and J.L. Reveal, 133-38. Pittsburgh: Carnegie-Mello n University Press.
. 1981b . Th e latera l displa y o f fishes: Bluf f o r honest y i n signalling ? Behav. Anal.
Lett. 1 : 233-35.
. 1981c . Some comments on sociobiology. Au k 98 : 412-14.
. 1982 . The patter n o f vocal signals and th e informatio n they convey. Behaviour 80:
1-8.
. 1983 . This week' s citatio n classic : The importanc e o f certain assemblages of birds
as "informatio n centers " for foo d finding . Current Contents 15 : 26.
26O BIBLIOGRAPH
. 1985a. Evolution of group life with special reference to the Arabian babbler (Turdoides squamiceps). I n Acta XVIII Con. Inter. Ornithol., ed . V.D . Ilyche v an d V.M .
Gavrilov 2: 1043 . Moscow: Academy of Sciences of the USSR.
. 1985b . Som e furthe r comment s o n th e gathering s o f birds . I n Acta XVIII Con.
Inter. Ornithol, ed. V.D. Ilychev and V.M. Gavrilov, 2: 919-20. Moscow: Academy of
Sciences of the USSR .
. 1987 . Th e theor y of signal selection an d som e of its implications. In Proc. Intern.
Symp. Biol. Evol, ed. V.P. Delfino , pp . 305-27. Bari, Italy: Adriatica Editrica.
. 1988a . Mat e guarding in Arabian babbler, a group-living songbird. Acta XIX Con.
Inter. Ornithol., 420-227. Ottawa .
. 1988b . Mat e choic e throug h signals . Acta XIX Con. Inter. Ornithol, 956-60. Ottawa.
. 1989 . Arabia n babbler . I n Lifetime reproduction i n birds, ed . I . Newton , 253-76.
London: Academi c Press .
. 1990 . Arabia n babblers : Th e ques t fo r socia l statu s in a cooperativ e breeder . I n
Cooperative breeding i n birds: Long-term studies o f ecology an d behaviour, ed. P.B .
Stacey and W.D. Koenig, 103-30. Cambridge: Cambridge University Press.
. 1991a . O n th e definitio n of sexual selection , Fisher' s model, and the evolutio n of
waste and o f signals in general. Anim. Behav. 42: 501-3.
. 1991b . Sexua l selection: Badges and signals . Tree 7: 30-31.
. 1993 . The fallac y of conventional signalling . Phil. Trans. R. Soc. Land. B 338: 227 30.
. 1995 . Altruis m a s a handicapth e limitation s o f ki n selectio n an d reciprocity .
Avian Biol. 26: 1-3 .
. 1996a . Th e evolutio n o f communal roosts as information centers an d th e pitfall of
group-selection: A rejoinder to Richner and Heeb. Eehav. Ecol. 1: 118-19 .
. 1996b . Cooperation among lions: An overlooked theory. Tree 11 : 252.
Zahavi, A., and D . Rait. 1984 . Socia l adaptations in myxobacteria. \nMyxobacteria, ed . E.
Rosenberg, 215-20. New York: Springer-Verlag.
Zahavi, T. 1975 . Socia l behaviour o f the babbler s (i n Hebrew). Hig h school project.
Zilberman, R. 1991 . Extra-pair copulation s in a sunbird population (Nectarinia osea osea)
in Ramat-Aviv area (in Hebrew). M.S . thesis, Tel-Aviv University.
Zuk, M. , K . Johnson, R . Thornhill, an d D . Ligon . 1990 . Mechanism s of female choice i n
red jungle fowl. Evolution 44: 477-85.
LIST O F F I G U R E S
8
261
262
LIST O F F I G U R E S
Toads 2
0
A sherif f i n a threatening stance 2
1
Dog 2
2
Terns, courtshi p feedin g 2
5
Crested newt with nuptial cres t 2
6
White pelican wit h nuptial bump 2
8
A stately country house 2
9
Satin bowerbird i n courtship 3
1
Peacock i n ful l displa y 3
2
Barn swallo w 3
3
Manakins dancing 3
5
White-collared ruf f i n display 3
6
Lyrebird i n displa y 3
7
Rooster 3
9
Red deer 4
0
Various species o f ducks in fligh t 4 3
Kangaroo 4
4
Babblers, mal e (above) and femal e (below ) 4
5
A decorate d plat e 4
7
Banded damselfis h 4
8
Danio zebr a fis h 4 9
Lesser black-backe d gul l 5
0
Feathers a t differen t stage s of wear 5
1
A peacock's feather with an "eye" 52
Butterfly 5
3
Convergencelong-claw pipit (Macronyx ) and meadowlark (Sturnella) 5
Red-backed shrik e 5
5
Cream-colored course r 5
6
Great ti t 5
7
"Status badges " 5
8
Lace collar, afte r Ruben s 5
9
Bengal bustard i n display jump 6
1
Bird o f paradise in displa y 6
2
Nestlings begging fo r foo d 6
3
Wolvesa dominant an d a subordinate 6
4
A foot rac e 6
5
Gray heron gettin g ready to fl y 6 6
Gazelle jumping playfully 6
8
Wolves howling 6
9
Shelduck chick 7
1
Crested lar k 7
6
Vervet monkey 7
8
List o f Figures 2 6
264
LIST O F FIGURE S
Babbler 14
1
Babblers aslee p on a branch 14
2
Babbler i n fligh t 14
4
Babblers fighting, grappling with each other 14
8
Babbler landscap e 15
0
Mutual feeding between ant s 15
1
Worker bee taking care of cells in a hive 15
3
A nest of Apis dorsata 15
4
Queen cell in a hive 15
6
A queen with her retinu e 15
9
A termite colony 16
2
A nest of Polistes canadensis 16
7
A pair of hawks 16
9
Stilts exchanging places at the nest 17
1
A male Alcichthys alcicoris taking care of eggs 17
2
Jacana 17
4
The lif e cycl e of cellular slime mold, afte r Bonne r 17
7
Dictyostelium, aggregating 18
0
Fruiting bodies o f Dictyostelium discoideum 18
2
A fruiting bod y o f the myxobacteri a Chondromyces crocatus 18
Scrub warbler feeding a European cuckoo nestling 18
5
Eggs of European cuckoo and its hosts 18
6
Cuckoo nestling pushing out a reed warbler's egg 18
7
Great spotte d cuckoo 18
8
An armore d knight 19
0
Cowbird 19
1
Dog eating food provided b y its master 19
3
Bacteriophage T4 19
4
Sandgrouse gathering at a water source 19
7
Breeding colony of black-faced dioch s 19
9
Rooks 20
0
Gulls divin g at food 20
2
Flock o f starlings near a roost 20
5
Hairdo, after Leonard o 20
9
A painted ey e 21
0
Heavy eyebrows, afte r Leonard o 21
1
A baby's face an d a n elderly face 21
2
Masksa witch an d a clown 21
3
The ideal womannow 21
4
The ideal womanthen 21
5
A ribbon aroun d a woman's neck 21
6
Lovers' hands 21
8
List o f Figures 2 6
Porcupines copulatin g 21
9
Alex the gra y parrot 22
1
Cave painting 22
3
A painted fac e 22
4
Donation box 22
7
INDEX
267
268
Index
Altruism (continued}
131-3, 149-50, 158, 161 , 230 ; gain from, 167 , 179 ;
and grou p selection theory, 161 ; host an d parasite,
240 n 20; in human, 225-7; and kin effect , 166-7 ;
and kin selectio n theory , 164; between non-kin , 163 ;
among parents, 171 ; and prestige , 144; reciprocal,
132-5, 149, 153 , 163 , 171 ; a s a signal, 150; in social
insects, 157-8 , 163 ; stalk formation, social amebas,
183; and suicid e (social amebas), 178-9; theories
explaining, 131-33; as threat substitute , 141-3, 149 ;
warning calls, 12
Amasa (Bible) , 213
Amboseli, Kenya, 77
Ameba, social. See slime molds
Amphibians, 25, 35
Amplifier signals , 56- 8
Amplifying differences , 56 , 58
Analog measuring, and nonverbal vocalization , 244 n
19
Anava, A., 73, 127 , 13 9
Andersson, M., 39
Andrena sabulosa, 190
Animals (general): large groups, 244 n 18;
performances, 34; and symbolic language, 77-80, 221;
vocabulary, 72, 78
Anis, groove-billed, Crotophaga sulcirostris, 148
Ankle, 217
Ant: 15 1 fig; aggression toward kin, 165 ; evolutio n of
social life , 151-4 , 162-3 ; as large social groups, 244
n 18 ; and noxiou s chemicals, 22 ; workers leaving
mother's colony , 241 n 30 Antelope, 48-9, 8 6
Anthropomorphic models : alcoholi c beverages , 103;
ballet dress, 96; boxers, 10-11; children jeering, 8;
contests, 46; crested helmets, 85 ; discussion of , 9;
drinking alcohol, 160; and evolution, 60 ; eyeliner, 45;
girlfriend leanin g on boyfriend, 116 ; gymnastics, 34 5; humans an d dog s a s partners, 193 ; human
information centers , 203; hunting estates, 29;
inflation, 59 ; inheritance laws , 123; knights an d serf s
as parasite and host , 190-1 ; littering, 132 ; longbow ,
82; Mafia mode l o f parasitism, 189; mansions , 29;
money (queen pheromone), 159 ; Olympi c games, 65;
ornaments that become cheap , 59; plate decorations ,
47; skydivers , 62
Anthropomorphism, 9
Antibiotics, 181 , 19 4
Antlers: XIV, 39, 55; evolution of, 89-90; as a
handicap, 87-8; i n ritual fighting, 62-3; an d social
rank, 14 4
Apes, 132 , 211
Aposematic coloration. See warning colors
Appeasement, 19
Arad, D., 183
Araiida, 30, 101
Arena: communal, mating, 199; leks, 34; of peacock, 33;
of sage grouse and ruffs , 2 5
Index
Baby: baby face , 213 ; "blackmail " by, 122 ; crying, 71,
121, 22 0
Bacillus, diphtheria , 19 4
Bacteria: antibiotics , 181 ; blackmail , 194 ; cAMP, 242 n
3; communal, 131 ; virulent an d non-virulent , 194
Bacteriophage T4, 19 4 fig
Bakal, C., 227
Balance: assumption of , 195; extortio n an d its cost, 122 ;
host/parasite, 185 , 192 ; mobbin g o f cowbirds, 191 ;
nestling begging , 189 ; powe r i n a group, 146
Bald head, human , 83
Ballet dress , 96 , 96 fig, 97 fig
Bangalore, India, 17 9
Bark: gazelle, XIII; babblers, 5 , 78
Barlow, J.W., 48
Barrette, C., 22
Bars, 16 0
Basolo, L.A. , 235 n 1 1
Bats, 2 9
Beak, 49-50, 53-4, 87, 235 n 25
Beard: human, 17 , 2D-4, 17 fig; ibex an d leopard, 87
Beauty, 46, 52, 214-5, 223, 225
Bedouins, 94-5 , 20 3
Bee, Andrena sabulosa (parasite) , 190
Bee, Apoidea: evolutio n o f social systems, 151-3,162-3;
large social group, 24 4 n 18 ; queen cell , 15 6 fig;
queen pheromone, 158 ; quee n wit h retinue , 15 9 fig;
threats b y noxious chemicals , 22; worker an d cells ,
153 fig. See also bumblebe e
Bee, honey , Apis mellifera, 153 , 16 0
Bee, Numada marshamella (host) , 190
Bee, stingless, Metiponmae, 15 4
Bee-eater, Merops apiaster, 82 , 9 9
Beech tree , 203
Begging, 63 fig, 189, 22 1
Behavior, human an d animal , 209-10
Behavioral mechanisms an d natural selection , 12-3 ,
120, 209
Belladonna, 211
Benefit t o th e group , 23 , 149 , 157 , 179 , 192 , 225
Betel nut, 160
Bible, 129 , 213
Bird o f paradise, king-of-Saxony , Pteridopbora alberti.
31,223
Bird of paradise, superb, Paradisaea raggiana, 61-2, 6 2
%
Birds of paradise, Paradiseidae: bristlin g feathers , 83;
leks, 35; males no t carin g fo r offspring, 31; tail, 25
Birdsong, 25, 28-9, 72 , 223, 236 n 2
Birdwatching, 67, 205-4
Bizarre signals, 38
Black, use of, 54, 94-7, 20 2
Blackbird, red-winged , Agelaius phoeniceus, 98
Blackbird, Turdus merula, 43, 97
Blackcock. Se e grouse, blac k
Blackmail, 120-2 , 194
269
27O
Index
Calls (continued]
threats, 19 ; warning, 74. See also vocalizations,
begging
Camouflage, 201, 237 n 2
cAMP, 180 , 183-4 , 242 n 3
Canvasback, Ay thy a valisinaria, 191
Carbon monoxide , 10 8
Care of young: forced, 189; fo r prestige, 171- 2
Caregivers: dependence on, 152 , 24 1 n 27;
manipulation by , 154
Carlisle, T., 127 , 137- 8
Carmeli, Z., 127 , 13 9
Caro, T.M., 232 n 7
Carotenoids, 93
Cask, 85
Cat, Felts silvestris, 69, 77, 120-1, 12 0 fig
Catbird, Australian, Ailuroedus,115
Catch-22, 38-9
Caterpillars, 9 fig
Cave paintings, 224
Cavy, Patagonian. Se e mara
Cell membranes, 230 , 242 n 3
Cells, 52, 10 7
Cellular slim e mold. See slime molds
Charity, 227. See also donation s
Cheating; chemical signal, 184 ; clothing , 217; an d
conventional signals , 58; cost o f signal, 212; hos t an d
parasite, 37; manes, 84; mimics, 9-10; i n morphs, 36 37; prevented b y pattern of signal, 24; quee n
pheromone, 159 ; and reductio n i n cost, 59;
ritualization, 64; stretching, 18
Cheeks an d lips (human) , red, 214
Cheetah, Acinonyx jubatus, 3 fig, 67
Chemical signals : cAMP, 242 n 3; communication an d
handicaps, 30, 101-8 ; differentiation, 178, 181 ;
evolution of , 108 ; harmfu l chemical s an d humans ,
160; on membranes, 230; in multicellular body, 107 8; queen pheromone , 158-60 ; signal and non-signal ,
184
Chick: extortion o f care by, 51; food bottleneck an d
female dominance , 174
Chickadee, Pams atricupillus, 148
Child: interes t in parent's reproductio n (ki n selection),
238 n 2; parent-child conflict , 119-21 , 124
Children: benefiting, 225; games, 8, 115; in human
families, 217; testing the bond, 111 , 115 , 119-24,21 9
Chimpanzee, Pan troglodytes, 63, 122 , 13 1
Chin, human, 213
Chromosomes, 153 , 162 , 19 4
Cicadas, 25,29
Cichlid fish , 1 8 fig
Cichlid fish, Cyrtocara eucmostomus, 31
Cichlid fish , Geophagus surinamemis, 16, 1 6 fig
Clothing, 46, 215- 7
Clown, 21 3
Clumping, 115-7 , 143 , 11 1 fig, 115 fig
Clutton-Brock, T.H., 2 9
Coalitions: babblers, 129 ; relatives, 166 ; socia l insects ,
154
Cock. See rooster
Coexistence, 19 2
Collaboration: evaluatin g interest, 158 ; hos t an d
parasite, 37; and human language, 217; humans, 182 ;
mating, 114 ; betwee n parents , 169 ; with relatives ,
166; socia l amebas, 182 ; socia l insects, 152 ; type s of,
148
Collaborators: human , 209, 217; parasite evolving into,
193-4
Colony: ant workers leaving, 241 n 30; gulls, 198 ; socia l
insects, 154-7 , 164-6 ; swallows, 199 ; termites, 241 n
27
Color: an d bloo d supply, 51, 93 ; bright, on eggs , as
extortion, 122 ; bright, a s a handicap, 235 n 36;
bright, an d predators, 30, 235 n 36; carotenoids, 93;
compromise, 98 ; and courtshi p display , 30, 32;
cryptic, 201-2; distinct, on body structures, 49-50;
and environment , 93-99; in forests, coral reef s and
kelp forests , 97; of fin , 19 ; glossy, 98-9; many , 96;
and parasites , 51; research on, 237 n 2; two, 50, 97 8, 234 n 14 ; of young, 121
Combination o f signals, 32- 3
Combs, 51, 81, 87, 93
Commands, 75- 6
Common interest , XIV , 5, 43
Communal children' s house, 210
Communal displa y at roosts, 204-5, 244 n 20
Communal nest, babblers, 129
Communal roost, 198-204 , 244 n 20
Communication: babblers, 126 , 222 ; chemical, 101-8,
184; child-paren t relationship , 124 ; differentiation,
178; and th e Handica p Principle , 209 , 229; betwee n
host an d parasite, 194 ; human language, 221-3;
between parenta l couple , 175 ; prey and predators,
XIII-XIV, 3-13, 23 2 n 11 ; and reliability , 70, 195 ;
between rivals, 15-24; between strangers , 222;
among unicellular organisms , 177; within th e body ,
52; wordless, 80 , 221- 3
Communities, as large groups, 244 n 1 8
Companionship, and sex , 220
Competition: over altruism , 13341 , 149 , 171-2 ; an d
genes, 162 ; gymnastics, 34; and th e Handica p
Principle, 40; human, 209; over mating and
breeding, 127 , 129-30 , 147 ; over mobbing, 141 ;
parents over caregiving, 171-2; and prestige, 125 ;
over reproduction , 142 ; and set-specifi c signals , 43,
46; socia l insects, 156- 7
Competitors, 204 , 227, 230
Complementary partners, 173
Compromise: in coloration, 98; between hos t and
parasite, 37
Comrades: opinions of, 226; a s rivals, 142
Confidence: an d staring , 55; in threats, 18
271
Index
Conflict: child-parent , 124 ; and concentration , 21, 236
n 10 ; escalation into fights , 15 ; between groups ,
babblers, 115 ; between informatio n collectio n
between gender s in mating, 26, 242 n 1 ; between
parents, 169 , 175; over reproduction, and quee n
pheromone, 159; resolution, 142; over territory, red
deer, 18-9 ; betwee n workers , 155-6
Conforming i n dress standards, 216; in threats, 23
Confrontations, between babbler groups, 11 5
Congregation, human , 203
Connection, logical , between signa l and message, 22930
Consciousness, 18 9
Conserving resources, through superterritories, 29
Conspicuous consumption , 160 , 227
Constraints: in gathering food for offspring , 156 ; in
host-parasite relationship, 188 ; on reproduction , 174;
over specific traits, 173
Constructions, animal, 31
Contempt, 21-2
Contests, 46
Conventional signals, fallacy of , 17 , 23, 58, 60, 159 ,
183,218,230
Convergence, 53-4, 54 fig
Cooperation: with competitors, 230; degree of , 111; in
defense o f territory, 113, 125; between do g and man,
193; amon g female babblers, 145 ; between genders ,
173; between hos t and parasite , 194; humans, 209,
217, 222, 230; among male babblers, 147 ; between
parents, 169; with raptor, 12 ; with rivals, 60; among
social insects, 156-7
Cooperative animals , 149
Copulation: o f babblers, choice of male, 145-7, 170 ; o f
babblers, new female, 129; of babblers, subordinate ,
147; competition over , in babblers, 147 ; and degre e
of dominance , 141 ; extrapair, 171; and male
caretaker, 172 ; no t for reproduction, 218-9 , 219 fig;
shyness about, babblers,145, 225; and wintering
pairs, 197. See also sex
Coral reefs, 44, 48, 97
Cormorant, Phalacrocorax, 97
Corvids, and cuckoo , 188
Cost-reducing traits, 88
Cost: of altruism, 144 , 150, 226-7; balance o f cost an d
gain, 189; importance o f in signa l selection, 59; of
low-pitched threat , 19-20; reducing, 88; and
reliability of signals, 58, 212, 189; search for, XVI; o f
signals and non-signals, 59-60; specific, in threats ,
16, 24; in time , 28
Goto Doana, Spain, 200-1
Courtship, 25^0; aggression, 31,113-4; colors, 30, 32;
conflict in, 26; constructions, 31,3 1 fig; dancing, 32,
34, 62; ESS, 233-J n 43; feeding, 25 fig; gift-giving,
32; of great crested grebe, 64; Handicap Principle in ,
40; and, parenting couple, 169; scents (pheromones),
30; showing ability, 28; testing interest, 114 , 11 4 fig;
Crabs, 31
Cracidae, 8 5
Creationism, 91
Crests, 84-5
Crickets, 25, 29
Cronin, H., 23 3 n 39
Crow, hooded, Corvus corone, 172, 187-9, 198- 9
Crows, Corvus, 141, 188
Cryptic colors, 11 , 201-2
Cuckoo, European, Cuculus canorus, 185 fig, 186-7,190
Cuckoo, great spotted, Clamator glandarius, 172, 18790, 18 8 fig
Curassow. See Cracidae
Cursor, cream-colored, Cursorius cursor, 55, 56 fig
Cuticle, 9 , 103
Cyrtocara eudnostomus, 31
Damselfish, banded, Dascyllus aruanus, 48 fig
Danaidae, pheromones of , 10 1
Dance: babblers , 117, 127, 143; bustards, 85; cost in
time, 28; courtship signals, 32, 34; group, 116;
group, humans, 117; manakins, 35; sage grouse and
ruffs, 2 5
Dancers, ballet, 96
Dancing arena, 25, 114 . See also leks
Danger an d fame, among human, 226
Danio zebr a (fish) , 4 9 fig
Daphne Island, 235 n 25
Darling, F.F., 22, 87, 198
Darwin, Charles: mimicry and huma n language, 77;
sexual display, 37-38; sexual selection, 38, 40, 44,
91, 233 n 42; singing, 70; social insects, 151-2, 164
Darwinian logic, and evolutio n o f altruism, 125
Daughter, inheriting, 124
Davies, N.B., 20, 186
Davis, G.W.F., 241 n 26
Dawkins, R.: arms race, 185; competition betwee n
genes, 162 ; evolutionary models, 239 n 17 , 241 n 26;
kin selection , 165; "mind reading" , 66
Decorations: as amplifier signals, 57; bowerbirds, 31-32,
114; decreasing apparent size, 237 n 10; emphasizes
features, 48; evolution of, 47, 47 fig; feathers, 31,91,
223; function of, 43; human, 211, 215-6; and their
message, 54; prove status, 56; selection of, 223-4; and
social status, 55; and symmetry, 52
Decoys, 231
Deer, Cervus: antlers, 55, 87-9, 144 ; courtship roars , 29
Deer, red , Cervus elaphus: courtshi p roars exhausting,
29; 40 fig, 92 fig.; fighting between simila r rivals, 22;
threats among, 15, 18-1 9
Defense, o f territory, 113, 173-4, 197-8 , 219, 234 n 44
Definitions: o f altruism, 161; of fitness , 162 , 165; of
handicap (sports) , XIV; o f prestige, 143^; of queen
272
Index
Definitions (continued]
pherormone, 240 n 13 ; of sexual selection, 38; of
signal selection an d utilitaria n selection, 40; of
signals, 59
Degree: of control, in babblers, 146-7 ; of cooperation ,
111; o f dominance, i n babblers, 141 ; o f emotion, 22 2
Dependence: o n caregivers, 152 ; on group mates , 115
Descendants, 162 , 192 . See also offspring
Deserting a mating partner, 170 , 219
Deterrence: of pursuit, 232; and the runawa y process,
39; and sexua l selection, 38; and song , 15. See also
intimidation; threat s
Development: o f human breasts, 215 ; perfection in , 33;
symmetry in, 52. See also evolutio n
Dexterity, 211
Dhondt, A., 29-30, 72
Dialogue, in singing, 76
Diamond, J.: colo r i n mixed-species flocks , 97 ; humans
and harmfu l chemicals, 160 ; menopause , 12 3
DIF, 179 , 181- 3
Differentiation, i n multicellular organism, 178-9 , 181
Digestion, of sugars and protein s i n wasps, 240 n 14
Digital measuring , i n verbal communication , 244 n 19
Dioch, black-faced, Quelea quelea, 198, 19 9 ( fig.)
Diphtheria, 19 4
Diploid, 15 3
Direction o f gaze. See gaze
Display: of disregard towar d predators , 235 n 36;
flights, 34; in flock, 205; leks , 34-5; o f status, 56; of
wealth, 60
Diving, larks, 62,
DNA analysis , 33, 127 , 130 , 172
Dog, African hunting, Lycaon pictus: 1 fig; groupbreeding, 131 ; group rituals , 117; observing stot ting, 7
Dog, Canis familiaris: friendly , 62; hair raised in threat ,
18; partnership with humans, 193, 19 3 fig; scolded,
61; showing contemp t i n threat, 22, 22 fig; testing
the bond, 111-2, 117; an d verbal language, 80, 80 fig;
vocalization of , 6 9
Dog, commo n red , Cuon alpinus, 9 8
Dolphin, bottlenose , Tursiops: ange r calls and posture ,
70; and verbal language , 80, 221
Dominance: bumblebees , 24 1 n 41; displayed by rape,
220; between mates, 173- 5
Dominant babbler : allofeeding , 137-8 ; copulations,
129, 145 ; mate-guarding , 170; mobbing, 139-41 ;
sentinel activity, 134-6; sleep, 143
Dominant individual : degree o f control, 146 , 147 ;
identified b y scent, 30; larger nose, 213; prestige, 149 ;
prestige an d altruism , 144-5; in social hierarchies, 22;
threats, 142 ; workers, 155
Donations, human , 160 , 226-7
Dove, turtle, Streptopelia turtur, 34, 62
Doves, communa l roost, 19 8
Drill, 216
Index
Evans, M . R., 34, 82
Evolution: altruism , 125, 149 , 150 , 158 , 161 , 230 ;
antibiotics an d toxins , 181 ; o f art, 223-5; bizarre
signals, 38; "blackmail" systems, 122 ; chemica l
signals, 108 ; constraint s on specific traits , 173 ;
decoration, 47 ; of decorative markings , 223;
definition, 161 ; ethics , human , 225; experiments ,
social amebas , 178 ; experiments, unicellula r
organisms, 60; of feathers, 90-1; grou p living , 147 ;
group-specific markers , 43-60; and the Handica p
Principle, 230 ; horns an d antlers, 89-90; kin effect ,
166-7; and kin selection theory , 163-5; markings, 53;
"not ye t complete," 191 , 195 ; parasite-hos t
relationship, 185-6 ; of parasitism into collaboration ,
193; polymorphism , 53 ; "psychological weapons, "
120; reproduction, 123 ; ritualized signals, 68;
runaway process model, 38; signals, 59, social
insects, 151-^, 162-3; "spiritual" needs, human , 224;
status badges, 56 ; 235-6 n i l, 236 n 36; of style of
clothing, 215; symboli c language in humans, 222;
unicellular organisms, 177
Evolutionary stable strategy . See ESS
Evolutionary systems, and huma n systems , 60
Evolutionary theory, and the proble m o f altruism,
161
Exaggeration: ritualization, 67; runaway process model,
39
Exploitation: o f offspring b y parents, 123 , 153 ; o f one's
mate, 169 , 175 ; by parasite of host, 185 ; betwee n
partners, group selection , 131 ; amon g social amebas ,
182; amon g socia l insects, 124 , 152^1 , 157 ; of
weaker partners, 152-4, 157
Expression, huma n facial, 214, 22 4
Extinction, 20 3
Extortion o f care, by self-endangerment: by humans,
220-1; by offspring, 120- 2
Extrapair copulation , 33 , 170- 1
Extravagance, 39, 40
Eyelashes, 212
Eyelid, 212
Eyelike pattern: fins, 50; peacock, 32-33 ; status badge,
55; value and widespread us e of, 52-3, 5 2 fig
Eyes: human, 210 fig, 212; movements, 55, 59; ring, 55,
59; sensitivity to color , 237 n 2; stripe an d directio n
of gaze , 55, 5 6
Face, human , 212 fig, 213-4, 224, 224 fig
Facial markings, 55, 213
Falcon, Falco, 12 fig, 34
Fame, 226
Family business, 165
Fanshawe, J.H., 7
Faran, N., 127
Fat reserves , 103, 215
Fatty acids: cuticle, 103 ; myxobacteria , 182; quee n
pheromone, 16 0
273
274
Index
Index
definition o f (i n sport) , XIV ; i n fighting , 87 ; i n
game o f tag , 8 ; gil l cover s hel d open , 66 ; horns ,
88; huma n bab y crying , 121 ; huma n body , 211-7 ;
key t o reliabilit y i n threats , 16 ; long tail , 83 ;
manes, 84 , 237 n 10 ; necktie, 217 ; ne w bod y
members, 91-2 ; no t physical , 57; no t random , 92 ;
proboscis, 87 ; pupi l size , human , 210-1; quee n
pheromone, 159 ; relaxatio n i n threat , 20 ; ribbo n
on neck , 216 ; ritua l fighting , 63 ; selectio n fo r
(signal selection) , 230 ; i n al l signals , 58 ; i n singin g
(time), 28 ; vision , 84- 5
Handshake, 117
Haplodiploid gende r determination , social insects, 153,
162
Hare, Lepus capensis, 121
Harmful chemicals : DIF, 181 ; an d humans, 160; quee n
pheromone, 158-6 0
Harmony, in birdsong, 223
Harriers, Circus, 126, 14 8
Hartwell, L.H., 10 4
Hasson, O. , 7 , 57, 232 n 11
Hatzeva, Israel , XV, 4, 15, 77
Hawaii, 70
Hawk, Galapagos , Buteo galapagoensis, 148
Head: apparen t size , and mane , 83
Health, durin g molt, 33
Heeb, 244 n 20
Heinrich, B., 199
Help: asking for, through suicid e attempts , 220-1, 226;
in kin selectio n theory, 161-2; in social amebas , 179 ;
unneeded, 164
Helpers: exploited offspring, 153 ; helpin g more than
necessary, 164 ; in a hive, 161; kickin g out husband ,
172; manakins, 35; partnership with kin, 165 ;
relatives, 162 ; sterile , and altruism , 241 n 21
Heredia, B. , 200
Heroism, 226
Heron, Ardea, 91, 123 , 171
Heron, gray, Ardea cinerea, 66 fig
Hesitancy, 55- 6
Hess, H.E. , 210
Hierarchies, 22 , 166
Hingston, R.W.G. , 237 n 2
Hiraldo, F., 200
Hive: compared to multicellular organism, 153; rank
and prestig e in, 160
Hoatzin, Opistbocomus hoatzin, 219
Hochberg, O., 77
Hoglund, J., 35
Holder, K., 81
Hlldobler, B., 165 , 241 n 30
Homosexuality, 219-20
Honesty, 16 , 24, 212, 230
Honeybee, giant , Apis dorsata, nest, 154 fig
Honk, C.G.J. , 160,24 1 n 41
Hoof, 49
275
Hook, 50
Hoopoe, Upapa epops, 8 4
Hopping, 34 , 62
Hormones, 107 , 215
Hornbill, Buceros, 85
Hornet, German . Se e Vespula germanica
Hornet, oriental . See Vespa orientalis,
Horns: color distinct , 49; evolution of, 86-91, 89 fig;
female, 90 ; male gazelle, 62- 3
Hospital, 16 0
Hosts and parasites : 185-95; acceptance by host of
parasite, 191 ; altruism , 240 n 21; bees, 190 ;
constraints, 188 ; Europea n cucko o genets, 186 ; hosts
showing themselves to parasite , 192; Mafia model,
189-92; neutering, 192 ; partnership, 37, 193-4;
prestige, 188 ; reproduction , 185 , 19 5
Hugs, 21 8
Hultsch, H., 76
Humans: 209-27; actor s an d credibl e threats , 20;
aggressiveness an d resolvin g conflicts by threats, 15 6; altruism , 150, 226 ; ar t an d decorations , 223-4,
223 fig, 224 fig ; assessmen t o f anima l signals , 34;
alcoholic beverages , 103 , 160 ; baby , 121-2 ; bal d
head, 83 ; beard, 17 , 213; body , 210-6, 21 3 fig, 214
fig, 216 fig; boxers, 17 ; breasts, 215; cAMP , 242 n
3; conspicuou s consumption , 227 ; cultura l an d
economic developmen t an d evolutionar y systems,
60; differentiatin g morphs, 36 ; diphtheria , 194 ;
dogs a s partners , 193 ; eyeliner , 45 ; eyes , 210 fig,
211-2, 21 1 fig; face, 212-3 , 21 2 fig, 213 fig; food
storage, 193 ; gende r an d reproductiv e constraints ,
219; grou p singing , 76 ; greeting, 117 ; hai r an d
dexterity, 20 8 fig, 211; Handica p Principle , 209 ,
230; huma n mal e features , 212, 216-7; human
female figure , 21 3 fig , 21 4 fig ; inces t avoidance ,
210; informatio n centers , 203-4 ; inheritanc e laws ,
123; li p color , 51 , 93 ; long neck , 216 ; lou d calls ,
74; lov e signals , 218; mal e aggressive stance, 17 , 2 1
fig; media attentio n t o aggression , 16 ; moral
behavior an d altruism , 225-7; menopause , 123 ;
nose, 86 , 213; observin g babblers , 133 ; pai d
enforcers o f rules , 23 ; pitc h o f threat , 20 ; postur e
and vocalization , 20; rap e an d dominance , 220 ;
reciprocal altruism , 132 ; rhythm , 73; self endangerment an d suicid e attempts , 220-1 ; se x an d
testing th e bond , 218-20; signa l selection , 40 ;
symmetry, 51 ; testin g th e socia l bond , 217-23 , 21 8
fig; threat b y voice , 21 ; threat s and audience , 75 ;
verbal language , 58, 80 , 221-3; vocal emotion, 236
n 5 ; waist , 217. Se e also anthropomorphi c model s
Hummel, 8 8
Hummingbirds, 9 9
Hunter, P.M. , 60
Hunting estates , 29
Hunting, 175,231
Huxley, J.S., 64
276
Index
Iron, 194
Ishay,J.,240nl4
Jacana, Jacana jacana, 174, 17 4 fig
Jackson, C.L. , 104
Jay, Florida scrub , Aphelocoma coerulescens,\48
Jay, Garrulus glandarius, 77, 14 8
Jeering, 8
Jerusalem, cit y of, 46
Jewish sages, 226-7
Joab (Bible) , 213
Joshi, N. V. , 164
Judaism, 227
Judges, contests, 2 3
Kacelnick, A., 237 n 1 0
Kalishov, A., 127 , 13 8
Kangaroo, Macropus, 44 , 44 fig
Katsir, Z., 74, 127
Katzir, G., 44
Kelp forests, 97
Kemp, A., 77
Kenya, 77
Keto group, 16 0
Kibbutz, 117,21 0
Killing offspring , 147, 17 1
Kin effect , 166- 7
Kin selection. See selection, ki n
Kin: altruism and parasites, 163 ; aggression towar d kin ,
164; effec t o f altruism o n reproductio n of , 167 ;
human, 210, 211 ; offsprin g as question of , 165 ;
unneeded assistance , 164. See also relative s
Kissing, 117,21 8
Kite, red, Milvus milvus, 20-1
Kitsch, 224
Knights, as parasites, 19 0 fig , 190- 1
Krebs, J. R. , 66, 185 , 24 1 n 26
Kruuk,H., 11,6 7
Kudu, Tragelaphus, 8 9
Labor, and alcoho l tolerance, 16 0
Lace, 60, 60 fig
Lack, D., 54, 235 n 36
Lambrechts, M., 29-30, 72
Language-, human, 80, 220-3; verbal, and animals, 77 80
Langur, Presbytis entellus, 84, 171
Lark, crested, Galerida cristata: and convergence , 54 ;
76 fig; crest, 85 ; mimicry in calls , 77
Lark, desert, Ammomanes deserti, black color , 94
Larkman, T., 127
Larks: singing in flight displays, 25; dives, 62
Larvae, of kymenoptera: 154-5 , 158 , 193 , 24 0 n 14 , 241
n27
Law, human: incest, 210; inheritance, 123
Leader, N., 173
Index
Leaning, girlfriend on boyfriend, 11 2
Leks, 34-35, 199
Leopard, Panther a pardus : an d ibex, 87; killing of
offspring, 171 ; spots , 48; spots a s signal to prey , 11;
and vervet monkeys, 77
Lie detectors, 23 6 n 10
Life cycle, slime molds, 178, 18 3
Life expectancy , babblers, 12 8
Life strategy, and morphs, 36
Light, ultraviolet, 99
Lines. See stripes
Lion, Panthera leo: courtship roars , 29; cryptic
coloring, 11 ; group-breeding, 131 ; mane , 84
Lips, human, 51, 93,214
Listening, conflic t wit h concentrating , 236 n 10
Littering, an d reciproca l altruism , 132
Lizard, zebra-tailed, Calsaums draconoides, 7
Lizards, 126
Logic: in nature, and the Handicap Principle , 229-30 ;
in prey-predator interaction , 6-7; relationship s in
insect colonies , 156 , 16 1
Longbow, 82 , 88
Loomis, W.F., 183 , 242 n 4
Loren, Sophia, 213
Lorenz, K. : coral fish, 44; human aggression , 15
Losing prestige, at human fundraisers, 22 7
Lotem, A., 127 , 186-7, 190 , 24 3 n 4
Loudness: begging, 189 ; calls , 74
Lovers, human, 218, 221
Low-pitched threats , 19-2 0
Lundy, K., 127
Lying, and verbal language , 223. See also cheatin g
Lyrebird, Menura, 37 fig
Lythgoe,J.N.,237n2
Macaque, Macaca, 12 3
Mafia mode l o f parasitism, 189-90
Magpie, Pica pica, 55, 188 , 19 0
Makeup, 214
Male: advertising, 26; aggressiveness toward females ,
113; babble r life strategy, 129 , 145,147 ; gazelles, 62 3; hymenoptera, 153 ; in leks, 35; moths, 238 n 4; no t
caring for offspring, 31; parenting constraints, 169 ,
219; rivals, 234 n 44; and sexua l act, human, 220;
taking car e of offspring, 170- 2
Mallard, Anas platyrhynchos, 43, 50
Mammals: adaptations fo r sea , 148; altruism , 150 ;
cAMP, 242 n 3; gender roles, 169 ; leks, 35; sexual
display, 25; scents, 26, 30; weaning, 119-2 1
Manakins, Pipridae,3l, 35 , 62, 35 fig
Mane, 83-4, 83 fig, 213, 237 n 10
Manipulation, of larvae by caregivers , 154
Manor house, 29, 29 fig
Mantids, Mantodea, 5 3
Mara, Dolichotis patagonica, 7
Markings: as amplifier signals, 57; and directio n o f
277
278
Index
Necklaces, 216
Necktie, 217
Negev, 94-5
Nestling: cuckoo, 186-7, 189 ; feeding of, babblers, 137;
gaping, 62, 63 fig; recognizing parasites, 243 n 4; self endangerment, 220
Neuropeptides, 10 8
Neutering, 192
Newt, crested, Triturus vitatus, 26, 26 fig
Niche, ecological . See ecological niche
Night roost , 202. See also communal roost
Nightingale, Luscinia megarhynchos, 15, 76
Nipples, 215
Nisbet, I.C.T., 27
Nitric oxide, 108
Nonmonogamous species, 11 4
Nonverbal communication, 80, 221-3, 244 n 19
Nose, 6 , 86, 213, 213 fig
Notices (conventiona l signals), 58
Noxious chemicals , 22
Numada marshamella, 190
Nuptial gifts, 2 6
Nursing, 119-2 1
Nutrients, prespore and prestalk social amebas , 179-80
Nymphs, 241 n 27
O'Donald, P., 28
Observation: of babblers, 133; of babblers' fights to th e
death, 15 ; of features, 82; of prey behavior, 66; of
signals, 59; o f stotting, 7
Offspring: an d "blackmail, " 122 ; constraint s on
gathering food for, 156; dominant female, 175; early
in season, 191 ; and evolutio n o f altrusim, 125;
existing, 123 ; exploited b y parents, 123 ; extrapai r
copulation, 171 ; host care, 189; human, 209-11, 219,
230; as kin, 162; not crying , gazelle, 121; not one' s
own, investment in, 131-3; and parents, 119-24 ;
relations betwee n parents , 170 ; runawa y process
model, 38-9; selectio n o f father, 49 ; sexual
reproduction, 169 ; social insects, 152; widows, 172;
of workers, 155
Olympic games, 65
One-celled organisms . See unicellular organisms
Open spaces, 95
Opium, 160
Orange color, 98
Orangutan, Pongo pygmaeus, 84, 84 fig
Ornamental feathers , 62
Ornaments: becoming cheap, 59; marked, 32
Ostrich, Struthio camelus, 148
Osztreiher, R., 116 , 127
Outlining shape , 49
Ovaries, 15 9
Oviduct, 15 3
Owl, 6 fig, 86, 123
Owl, barn , Tyto alba, nestlings, 12 3 fig
Index
Paintings: 223-4, 223 fig, 224 fig
Pairbond, 116
Parasites: 185-95; accepting, to minimize damage, 191;
altruism of host, 240 n 21; arms race, 185-6, 195 ;
balance with host , 185 ; an d bright colors , 51; care
for, proving ability, 172 ; a s collaborators, 190, 193 ;
European cucko o populations, 186 ; grea t spotte d
cuckoo an d crows , 187 ; amon g kin, 163; less an d
more virulent, 194; neutering host, 192 ; recognizing
as nestling, 243 n 4; risk to nest , 152 . See also host
and parasite
Parasitism, social. See social parasitism
Parent-child conflict , 119-20, 124 , 238 n 2
Parental manipulation , 123 , 153 ^
Parents: babbler s an d adul t offspring , 128 ;
competition ove r caregiving , 171-2 ; exploitin g
offspring, 123 , 153 ; gende r constraints , 169 ;
genuine warnin g calls , 12 ; human bab y crying , 71 ,
121, 220 ; n o parenta l involvement , 27 ; an d
offspring, 119-24 ; parenta l couple , collaboratio n
and conflict , 169 , 175 , 18 9
Parker, G.A., 1 6
Parker, P., 127
Parrots, Psittacidae, 77, 80, 116 , 123 , 221, 22 1 fig, 244
n 17
Partner: aggression among, 240 n 5; babbler,
dependance on , 115 ; convincin g of quality, 171;
evaluating, 160 ; gai n by partnering with relatives ,
165; guardin g territory, 188; i n a hive, 157-8 ;
human, and bab y crying, 121 ; language and
cooperation, 222 ; mate and territory , 174 ; parasite
against other parasites, 190; prestige, 149 ; prestige,
babblers, 146 ; reciprocity, 134; showing off wealth,
227; strength of bond, 111 ; testin g the bond, 117 ;
weaker, and threa t o f self-injury, 120 , 220
Partnership: an d altruism , 172; babblers, ne w group,
130; breakup, crows, 188 ; complementar y partners,
173; group selectio n an d exploitation , 131 ; host an d
non-virulent parasite, 194; humans, 217-220;
humans and dogs , 193 ; insects, 152-4; with kin, 165 ;
new pair, 188 ; strengt h of, 112 ; testing the bond ,
same-gender, 220
Partridge, chukar , Alectoris chukar, 55
Paternity, guaranteeing, 170
Patriotism, 226
Pattern: emphasize s features , 48 ; eyelike, 50; human
beard, 213; selection of , 223; of threat, prevents
cheating, 23-4. See also markings
Payne, R.B., 77
Peacock, Pavo cristalus: color, 30; combination o f
signals, 32-33, 32 fig; courtship, 114 , 11 4 fig;
escaping predators, 33; eyelike patterns, 32-3 , 52-3 ,
52 fig; hen's preference , 33, 223; males not caring
for offspring , 31 ; tail XIV, XVI, 25, 34, 52, 55, 82,
144; waste, 150 , 15 7
Pecking order, 22 , 144
279
Peek-a-boo, 115
Peers, 204, 227
Pelican, Pelicanus, 50, 84
Pelican, white , Pelecanus onocrotalus, sexual display
(bump), 26, 28, 28 fig
Penguin with chick, 122 fig
Penguin, Humboldt , Spheniscus humboldti, 99 fig
Pepperberg, I.M., 244 n 17
Peptide, 104- 5
Peregrine, Falco peregrinus, 126
Perl, Y., 127 , 146
Personal space , 218
Pest control , 23 8 n 4
Pest, 189
Petri dish, 178, 180
Petrie, M., 33, 35, 52
Petting, 218
Pheasant, Pbasianus, 25
Phenotype, 107 , 182 , 186-7, 194
Pheromones, 30-1 , 101-2 , 104-7, 152 , 159-60, 238 n
4. See also queen pheromon e
Physical contest, 63
Physiology, human and animal , 209
Pigeon, passenger , Ectopistes migratorius, 203
Pigeon, rock , Columba livia, 174
Piglets, wild , Sus scrofa, 121 , 12 1 fig
Pilots, 216
Pioneers, 117 , 11 7 fig
Pipit, long-claw , Macronyx, 5 4 fig
Pitch, vocal , 19-2 0
Plasmid, 19 4
Plastic, 225
Plate, decoratio n of , 47, 47 fig
Playing. See games
Plovers, 85 , 171 , 17 5
Poison: i n butterfly pheromones, 30 ; DIP, 179 , 181-3 ;
queen pheromone , 158 ; warning colors, 9-1 0
Police, 23
Polistes biglumis, 193
Polistes canadensis, yellowjacket, 165-6 , 167 fig, 240 n 5
Polyandry, 170
Polygamy, 45, 16 9
Polymorphism, 36-37, 53-54
Ponzo's effect, 23 7 n 10
Population: crow , 188 ; huma n hair, 211; passenge r
pigeon, 203; reed warbler, 186 ; runawa y process
model, 38; social amebas, 178, 180 ; spread o f
marking in, 53^&; spread o f traits in, 230; traits
spreading through, 189; unicellula r organisms , 177
Porcupine, Hystrix indica, 83, 218, 21 9 fig
Posture: an d clothing , 46; and color , 30; and mood, 71;
and voice, 20, 69
Potlatch, 226
Pozis, O. , 127
Prayer, communal , 203
Precision, 29-30 , 216
28O
Index
Index
n 36; communication, babblers, 222; communication
between parental couple, 175 ; communicatio n within
the body , 52, 58; conventional signals , 58; in
courtship signals , 26; demanded b y observers, 59;
eyes, human, 212; friendliness, 62 ; genetic code, 58;
in hormones, 107 ; host an d parasite, 194-5 ; and
human language, 58, 221; human nonverba l
communication, 223; intent an d pupil size , human,
210; need for food, 122 ; red lips, human, 214;
selection for , 230; showing off wealth, 227; signals,
XIV-XVI; signal selection, 40; status badges, 56,
170; testing fo r committment, 218; testing the bond ,
112, 117 ; i n threats, 16 , 19; threats an d threa t
substitute, 142 ; vocalizations in chase, 9; vocal
signals, 69-70; and waste, 229
Religion, 217, 203 , 210
Repression, o f larvae, 152
Represser protein, diphtheria toxin, 194
Reprimanding, 14 5
Reproduction: an d altruism , 161; babblers, 129 ;
bottleneck an d femal e dominance, 174 ; chances of
social insects, 157; competitio n over , 142 , 159 ;
deserting a partner, 170; favor s "selfish " mutants, 23;
gender constraints, 169 , 219; of host an d parasite ,
185, 195 ; huma n gender constraints, 219; ki n
selection, 162 ; natural selection, 122-4 , 123 , 131 ,
151; i n other nests , ants, 241 n 30; parenting couple ,
169; parent/child an d kin selection, 238 n 2; parentoffspring conflict , 120 ; partnership wit h kin (socia l
insects), 165 ; and prestige , 145 , 158 ; ree d warble r
and Europea n cuckoo , 187 ; rhythmi c song, 30;
sexual selection, 38 ; species identification, 45; and
spread o f traits in populations, 230 ; and ston e
collecting, 173 ; and takin g care of others' offspring,
188-9; of workers, social insects, 153
Reproductive organs , attacked by parasites, 192
Reptiles; adaptations for sea , 148; morphs, 37; sexual
display, 25
Requests, 75
Reserves: of fat, 103; of glycogen, 182
Resolution o f conflicts, 15-6 , 142
Resources: of neutered host , 192 ; for surviving DIP,
182-3
Revolt, 137
Reward: for altruism , 139; for art , 224
Rhinoceros, Asiatic, Rhinoceros unicornis, 86
Rhinoceros, square-lipped, Ceratotherium simum, 86,
86 fig
Rhinoceroses, Ceratotherium, 63
Rhythm, 21, 30, 72^t
Ribbon, 216 , 21 6 fig
Richner, 244 n 20
Ring, around eye , 55
Risk: altruism and risk y activities among humans, 225 7; ensuring credible threat, 24 , 68; of fighting, 234 n
44; to kin, in kin selection theory , 164 ; to nest, 152 ;
281
282
Index
Sensitivity to color, 23 7 n 2
Sensory cells, 10 2
Sensory exploitation, 235-6 n il
Sentinel activity : babblers, 3 , 127 , 133-6 , 144-5 , 225, 4
fig, 135 graph, 13 6 graph; cost i n time, 28;
Serfs, 190- 1
Set-specific markers, 43-49
Sexual act, 117 ; forced, 220; not fo r procreation ,
animals, 218-9; same-gender partnerships, 220 ;
testing the bond, humans, 218-20;
Sexual display, 25-6, 37-8 , 22 9
Sexual partners, selection an d number, 169
Sexual reproduction, parenting couple, 16 9
Sexual selection. Se e selection, sexua l
Sexual showing-off, mathematica l models, 22 9
Shame, 226
Sharing: assets, human partners, 217 ; a territory, ma n
and dog , 193 ; territory, pair , 11 3
Shaulski, G., 183 , 24 2 n 4
Sheath, of beak, 87
Sheep, bighorn, Qvis canadensis, 63
Shelduck chick, Tadorna tadorna, 71 fig
Sheriff, 2 1 fig
Shouting, 74-5, 12 7
Showing off : ability as provider, to one's mate, 189 ;
ability, by waste, 157 ; abilit y and commitment , by
altruism, 158 , 172 ; abilit y to feed, 27-8; adaptation ,
by handicap, 57 ; by altruism, humans, 227; art and
imperfection, 224 ; by clothing, 216-7 ; by color, 93;
confidence, 56; confidence, by threat, 18 ; contempt ,
22; differences , 47; by donations, 160 ; lac k of
parasites, by color, 51; in large gatherings, 205; by
long neck, 216 ; motivation , b y pitch o f voice an d
stretching, 19 ; motivation, b y threat, 24; neatness, by
uniform, 216; perfectio n o f edge, by line, 47;
posture, b y color, 30; sexual, 229; status, to peer s
and competitors , 204 ; symmetry, by decoration, 48 ,
52; wealth, through mansions , 29; wealth, 227. See
also advertisin g
Shpirer, Y. , 187
Shrike, great gray, Lanius excubitor, 98
Shrike, red-backed, Lanius cristatus, 55 fig
Shrikes, Lanius, 4, 26-7, 5 5
Shushlui Nature Reserve, South Africa , 49 , 86
Shyness, babblers, 145-7 , 225
Siamese fighting fish, Eetta splendens, 6 5
Sibling: helping, 162 , 164 ; parent/child conflic t and ki n
selection, 23 8 n 2; preference, 123 . Se e also selection ,
kin
Side effects: antibiotic s an d DIP, 181 ; benefi t t o group ,
149; kin effect , 166 ; specie s identification, 57
Sigmund, K., 239 n 1 7
Signal selection. See selection, signa l
Signals; acetate , acid , alcohol , aldehyde , 102 ;
altruism, 149-50 ; betwee n experience d co-workers ,
222; chemicals , signa l an d non-signal , 184 ; clarit y
Index
of, 64 ; combination s of , 32 ; conventions , 58 , 218;
correlation t o quality , runawa y proces s model , 39 ;
cost an d message , 229-30 ; cres t an d mane , 84 ;
definition, 59 ; deterren t t o pursuit , 23 2 n 11 ; DIF
not a signal , 182-3 ; evolutio n of , 23 5 n 36 , 235- 6
n 11 ; ey e movemen t an d markings , 59 ; an d
handicaps, 57 ; huma n bod y fa t an d breasts , 215 ;
human bod y parts , 212-7 ; huma n clothing , 216;
human hair , 211 ; markings an d arbitrariness , 47 ,
53; o n membranes , 230 ; menstruation, 214;
neuropeptides, carbo n monoxide , nitri c oxide ,
toxic chemicals , 108 ; observation of , 59 ; b y
predators t o prey , 8-11 ; b y pre y t o predators , 3 10; quee n pheromone , 159-60 ; receive r an d
reliability, 229 ; reliability, XIV , 229; ritualized
movements, 67-8 ; set-specifi c markings , 43 , 58 ; a
signal o r no t a signal , 82 ; signa l selection , 40 ;
status badges , 56 ; threats , 17 , 24
Simpson, M.J.A. , 65
Sinai, 94-5, 172 , 203
Singing: and abilit y to feed , 28; courtship signals , 32;
Darwin, C. , 70; sexual display, 25; showing abilit y to
escape, 8 ; threats, 15 ; as waste, 39
Size, apparent, 213, 237 n 10
Skill: and art, 224; an d long hair , 211
Skin, exposed, and heat loss, 214
Sky divers, 62
Skylark, Alauda arvensis: singing in escape, 8; wing
load, 88; white color , 94
Slagsvold, T., 14 1
Slime molds (socia l amebas), Dictyostelmm discoideum,
131, 177-84 , 177 fig, 242 n 4, 18 0 fig, 182 fig
Slug (aggregat e of social amebas), 178-9, 182- 3
Smith, H.G., barn swallows , 33-34
Smith, J.N.M., 191
Smith, N.G., gull species identification , 44
Smythe, N., 7
Snakes, mobbed by babblers: 79 , 126 , 133, 139, 139 fig
Sober, E., 241 n 33
Social amebas . See slime mold s
Social behavior: and environment , whit e wagtail, 198;
of humans, and the Handicap Principle , 209
Social bonds: XVI , 111, 113, 117, 217-23
Social hierarchies , 22
Social insects : 150-67 ; aggressio n amon g kin, 164;
altruism, 179; basic problem, 152 ; colony formation,
154-5; exploitation , 124 ; food gatherin g constraints ,
152, 156 ; gender determination , 153 ; group selectio n
and altruism , 161; kin selection an d haplo-diploid
mechanism, 162 ; small colonies , 158; social parasites,
157
Social parasitism, 131 , 157, 163
Social rank. See rank
Social standing: humans, 216, 226-227'. See also prestig e
Social status, an d markings , 55. See also prestig e
Social structure , evolution of , social insects , 154
283
284
Index
Stresemann, E., 94
Stretching, 18- 9
Stripes, 48, 55, 121 ; through eye , 55
Struggle: among kin, social insects, 165; among workers
in a hive, 156-7; minimizing damage, 192
Style, 46-7,215, 217,225
Subordinate, 56, 143 , 149, 212
Sugars: digestion, in wasps, 240 n 14 ; in glycoproteins ,
105
Suicide, 178, 220-1, 226
Sulcopolistes artimandibularis, 193
Sunbird, Palestine, Nectarinia osea, 171
Sunbird, scarlet-tufted malachite , Nectarinta johnstoni,
34,82
Sunbird, yellow-bellied, Nectarina venusta, 28
Sunbirds, Nectarina: color , 30; glossy color, 99;
mobbing raptors , 5
Sunfish, bluegill , Lepomis macrochims, 36
Superterritories, 28- 9
Surgeonfish, Zebmsoma, 50
Surrogate mother, parasite and host, 191
Survival: lon g hai r a s a handicap , 211; nee d
for cooperation , socia l insects , 157 ; and DIF ,
180-3; socia l amebas , 179-80 ; tin y rate , o f young ,
151
Swallow, barn, Hirundo rustica, 33, 33 fig
Swallow, cliff , Petrocbelidon pyrrhonota, 199
Swallows, Hirundo, communal display at roost, 204;
individual space, 116, 116 fig; long tail, 82;
symmetry, 51
Swan, black, Cygnus atmtus, 98 fig
Swan, Cygnus olor, 96-7
Swarm, 156, 198
Symbiosis: compared t o collaboration wit h relatives,
166; and th e Mafi a model , 193
Symbolic language, human, 221-2
Symmetry, 48,51-3,223
Synchronization and eyelike pattern, 53
Synchronization, of development, 52-3
Taborsky, M., 233 n 36
Tag game, 56
Tail, 25, 33^, 49, 53, 55, 82, 144
Taste, clothing , 216
Tastelessness, 22 4
Tel-Aviv University zoo, 85
Termites, hoptem, 151 , 153, 162, 162 fig, 241 n 27, 244
n18
Tern, Sterna hirundo, 25 fig, 26-7, 82
Territory: babblers , 4 , 125 , 127-9, 131 , 147-8 ;
crows, pai r cooperation , 188 ; dark ruffs , 54 ;
defending b y threats , 23 4 n 44 ; defens e of , an d
dominance betwee n genders , 173-5 ; givin g up , 16 ;
miniterritories, 34-6 ; morphs , 37 ; pair , 113;
parasite, 190 , 192; prehistoric humans , 211;
readiness t o protect , 15 ; shared b y human s an d
Index
relationship, 119-20; reciprocal altruism theory, 132,
163
Tropicbird, Pkaethon aethereus, 34, 82
Tufts, 8 6
Turkey, Meleagris gallopavo, 51
Ultraviolet light, 99
Unconscious, behavior mechanisms, human, 210
Uneven cost, 58
Unicellular organisms, 60, 150 , 177-8, 184
Uniforms, 216
Unpalatable prey, 9
Unsaturated fatt y acids , 101 , 160
Utilitarian selection. See selection, utilitarian
Values, spiritual, 224
Vandal, D., 22
Veblen, T., 160 , 203-4, 227
Verbal language : animals , 77-80, 221; humans, 221-3 ,
244 n 1 9
Vespa orientalh, oriental hornets: 155 , 240 n 14
Vespula germanica, German hornet , 155 , 240 n 7
Vidua, Vidua, 2 5
Vigor, related t o attractiveness , 233 n 42
Violence, 16 0
Viper, Vipera, 5 4
Virulence, 194
Viruses, 194
Visibility as a handicap, 235 n 3 6
Vision: handicaps to, 84-5, 211; monocular, 55
Vocabulary, 72
Vocal emotion, human, 236 n 5
Vocalization: 69-80; babbler research , 127 ; in a chase,
9; courtship, 29-30; distance , 20-21; and emotion,
222; message, 71; mimickry, 77; pattern an d it s
message, 72; reliability, 69-70; threats 19-20 ; and
verbal language, 244 n 19 . See also call s
Voice: an d posture, 69 ; quality of, 222; concentration,
236 n 1 0
Vulture, Egyptian, Neophron percnopterus, 202
Wagner, R., 87, 199
Wagtails, Motadlla alba: roost, 202, 204; social
organization, 197-8; wintering pairs 113 , 113 fig,
219
Waist, 217
Wallace, A.R., 44
War paint , 39
Warbler, great reed, Acrocephalus arundinaceus, 186-7
Warbler, scrub , Scotocerca inquieta, 185 fig
Warbler, Seychelles , Acrocephalus sechelensis, group
living, 14 8
Warbler, Sylvia, 5
Ward, P., 198 , 243 n 4
Warmth, 199
Warning calls : babblers, 3 ; genuine, 12 ; loudness, 74 ;
285
2 8 6 Index
Wrinkles, facial, human , 213, 22 4 of
Wynne-Edwards, V.C. , 203^ 1 askin
, 203
, T., 127 , 13 4
, Equus, 48, 98
m game , 14 9
, R. , 171
, M. , 51