Why Males Exist PDF

WHY
MALES
EXIST
AN INQUIRY INTO THE
EVOLUTION OF SEX
by FRED HAPGOOD
WILLIAM MORROW AND COMPANY, INC.

NEW YORK 1979
To the fathers of ethology:
Julian Huxley, Karl von Frisch,
Komad Lorenz, and Nino Tinbergen
Copyright © 1979 by Fred Hapgood
All rights reserved. No part of this book may be reproduced or utilized

in any form or by any means, electronic or mechanical, including
photocopying, recording or by any information storage and retrieval
system, without permission in writing from the Publisher. Inquiries
should be addressed to William Morrow and Company, Inc., 105 Madi-
son Ave., New York, N. Y. 10016.
Library of Congress Cataloging 10 Publication Data
Hapgood, Fred.
Why males exist.
Bibliograpby: p.
Includes index.
1. Sexual behavior in animals. 2. Reproduction. 3. Evolution.
I. Title.
QL761.H36 591.5'6 79-13805
ISBN 0·688'()3546·9
Printed in the United States of America.
First Edition
1 2 3 4 5 6 7 8 9 10
ACKNOWLEDGMENTS
My GREATEST DEBT IS OWED TO THE ETHOLOGISTS WHO

brought back the stories that light up these pages. Unfortu-
nately, they are far too numerous to mention individually; even
my bibliography does not do them justice. The professional
literature is amazingly rich. I cannot count the times I opened
a journal in search of a specific reference and found myself
reading one article after another, each more wondrous and
delightful than the last. I tried to convey some feeling for
these reports by quoting from them frequently.
A second debt is owed to certain specific theoreticians and
scholars. Preeminent among these is Ernst Mayr, whose
magisterial book, Animal Species and Evolution, gave me
more instruction and excitement than any other book I can
recall. E . O. Wilson's Sociobiology first revealed to me the
degree of skill and intelligence with which animals live their
lives. George Williams, in his Sex and Evolution, challenged
me to think about these problems, in large part by the style
of his example, which was one of great openness, honesty, and
modesty. Robert Trivers was very important in focusing and
supporting my energies on this subject. It is impossible to
imagine this book without the famous contributions that his
imagination, incisiveness and intellectual stubbornness have
made to behavioral biology. Michael Ghiselin's The Economy
of Nature and The Evolution of Sex were also extremely
instructive.
Finally, I wish to thank John Hartung, Frank Benford,
John Weinrich, Sandi Friedman, David Crews, Richard
Wrangham, Mrs. Tamsin H. Hapgood, Sara Dunlap, Steve
Warshall, Mrs. Herbert P. Mayo, Yin McLellan, and Sarah
Hrdy for reading and commenting on the manuscript at vari-
ous stages.
CONTENTS
Acknowledgments 7
Introduction II
I. The Extravagance of Males 15
II. The Rule of the Game 20
III. Living Sexlessly 25
N. An Overview of Some of the Cons and Pros of Sex 32
V. The Transition to Sex 35
VI. The Consequences of Being Sexual 53
VII. The Evolution of Gender 67
VIII. The Prisoner of Gender-an Unresolved Mystery 78
IX. Doing the Paperwork and Other Issues 84
X. Male Society-the Society of Competition 98
XI. Female Influences on Male Society 110
XII. The Cost of Male Competition to Females 128
XIII. Males With an Edge 139
XN. Male Leverage and Equality 149
Notes 189
Index 201
About the Author 213
INTRODUCTION
THIS BOOK HAS TWO AMBITIONS: ONE EXPLICIT, ONE IMPLICIT.

The explicit intention is to present a problem that few peo-
ple know even exists, and that is the mystery of males, why
they're here and what they're for. The dilemma is best stated
with an illustration. Grizzly bear females carry, nurse, pro-
tect, and train their young. Male grizzlies take no role in any
of these activities; they make no obvious contribution at all
to the energy needs of reproduction. All those burdens, such
as having to hunt and forage for a whole family instead of
just for one, fall onto the female's shoulders.
Given that fact-and this arrangement is very common in
nature-what good are males at all? Why did they arise, or
evolve, in the first place? There are many species that get
along perfectly well without them. Some of these reproduce
without using sex (that is, gene-mixing, or fertilization) at
all; in others, all the individuals make both sperm and eggs
and then reciprocally fertilize each other. Why are these al-
ternatives to males not more widely pursued? Why aren't we
all bisexual, with one gonad acting as a testes and one as an
ovary (only one of each is necessary for either reproductive
role anyway)?
Perhaps there is no good answer to this question. Males
may well be an evolutionary dead-end that will be abandoned
when another system, less parasitical on and wasteful of fe-
male energies, appears. But there are other possibilities, and
these can be summarized by saying that males might make
sense if they allow the needs and desires of females to con-
trol their actions.
The second, implicit, intention is to show that animals and
12 / WHY MALES EXIST
humans belong to the same culture. We humans are so flexible
in our behaviors, we are adapted to so many different environ-
ments, that there are very few species anywhere on the globe
that are not dealing with issues that are familiar and important
to us. To put the matter in its most egoistic form, human be-
havior summarizes that of all the members of the animal
kingdom. No doubt these few words have failed to define
this idea with any clarity, but there is no point in continuing
to press it in general terms. There is a te"t at hand, with lots
of examples, and the best definition is a good illustration.
Nevertheless all living things have much in common.
-CHARLES DARWIN
CHAPTER
I
THE EXTRAVAGANCE
OF MALES
WHAT IS THE DIFFERENCE BETWEEN THE LIVING AND THE

dead? between biological creatures, some as immobile as rock
and as passive as windblown sand, and inorganic substances
and reactions, some of which, like fire, can grow and leap as
responsively as most living things? This is an old question,
with many answers, but the answer that seems to work best
is: Living things can reproduce themselves. Dead material
loses its patterns with time; it erodes, crumbles, decays, dis-
solves. Living organisms can preserve their forms intact by
building them anew, over and over, and so pass themselves
down through time. Life is the power of changing substance
while preserving form.
It is as awe-inspiring, as overwhelming, as any of the other
natural powers. Our planet is heavy with forms straining to
stamp out copies of themselves, most of them trying to trans-
form the flesh of other life-forms into their own patterns.
Some naturalists celebrate this rank, riotous fecundity ; others
detect something driven and horrible at its heart. "In this rep-
etition of individuals is a mindless stutter, an imbecilic fixed-
ness • • . ," Annie Dillard, one of our best contemporary
nature writers, has written. We are concerned, in these pages,
with one small aspect of this fierce power, and that is the fact,
16 / WHY MALES EXIST The Extravagance of Males / 17
and the implications of the fact, that all this abundance (with season, being a male is an exhausting business that involves
trivial exceptions) is the work of females. competing continUOUSly with many other males.
In other words, among species with genders, it is the fe- Sometimes this competition takes the form of a direct phys-
males that have control over the reproductive cycle; the males ical attack by one male on another; most often it means noise,
appear to be virtually irrelevant. The single-parent family is
the rule in nature and that parent is almost always female.
a great deal of noise, produced nonstop, hour after. ho~r,
sometimes day after day. These are the sounds of musIc wIth
. (
It is the females that watch the environment to clock the which the hills are alive-the choruses of frogs; the shrieking
arrival of favorable conditions, secure the food to make and of the cicadas; the staccato calls of crickets; the repertories
nourish her eggs, find and/ or prepare a proper place to lay of male songbirds; the yowling of tomcats on the prowl. And
her eggs or leave her young, and incubate, nurse or feed, from the beIIowing of bull stags to the peeping of tree frogs
train, and protect them. By and large males take no part in all this sound serves the same ends; it intimidates rivals and
these activities. attracts and/ or persuades females. It is all huckstering and
There is only one wide-spread class of exceptions to this swagger matches; winning and losing; an endless game of
generalization; perhaps in 90 percent of the bird species the who's better.
! male shoulders a fair share of the reproductive responsibilities
-helping to build the nest, defend the site against competitors
and predators, and feed the young. In no other class of or-
So the fact that males are excluded from any real participa-
tion is reproduction does not mean that they have it easy; if
anything, their lives are harsher and more taxing than those
ganisms does the percent of species with working males rise of females. A biologist named Valerius Geist has measured
higher than 10 percent, and usually it is far less than that. To the skulls of mountain sheep and found that males with larger
draw a parallel, if females and males were partners in a con- horns died younger. He believes that the large horns bring
struction project, females would have to be imagined as put- males sexual success, but that that success has a cost. The
ting up the capital, hiring the subcontractors, acquiring the sheep have to constantly ward off threats by other males to
necessary materials, arranging for the permits, and devising "their" females. This destroys the fat reserves they need to
half the design changes. The males contribute half the design see them through the winter, and therefore sexuaIIy success-
changes and collect 50 percent of the profits-the same share ful males die earlier. Geist writes:
as the females.
This parallel is not quite fair to males; they cannot, in fact, Once rams have entered their period of dominance, of high
social success, of guarding and breeding with females, they
afford to loll about. Since males have only a peripheral role
begin to age and die rapidly. Mortality increases five- to eight-
in the reproductive cycle, it takes them virtually no time at all fold over that of younger, subordinate rams. Once they have be-
to reproduce-all they have to do is mate. That means that, come breeding rams, the males have not long to live.
at least theoretically, one male might be able to fertilize all
the females in a large area; an achievement that would shut all Sex can be shown to be bad for males in other ways as well.
the other local males out of reproducing altogether. Since, as There are: spiders that capture male insects by giving off
Darwin taught, natural selection chooses individuals that re- the odor of a receptive female; firefly predators that catch
produce better, one would expect evolution to produce males males by giving off the distinctive flash pattern of a female
who would go to great lengths to avoid being so excluded. firefly; cricket-hunting wasps that are attracted by the song
And so it has, with the result that, at least during breeding of male crickets. When wild dogs hunt gazelles they do so in
The Extravagance of Males / 19
a specific formation that makes it easy to catch any gazelle '1' ess and efficiency' when one looks at males one
progem \Yen t' azingly elaborate forms of wastefulness.
that tries to double back. They do this because often the sees the mos am th they
gazelle they are pursuing is a male whom they have chased w is it possible that both genders evolved toge er, as
from his mating territory, and who will be desperate to twist H~st have? And are males reaJIy what they seem ~o be, ~n
around and return to it. When he turns he is caught. To be m I ti' ary fn'volity an extravagance with no practical pornt
evou on ,
blunt about it, sex makes males do very stupid things; they to them at aJI?
seem to throw aJI concern for survival to the wind. And there
is a perverse logic to it aJI. Any male that tried to live a sober,
sensible, careful life might live for a long time, but he would
never reproduce. His rivals, the reckless bravos, might lead
short lives, but they would be full ones, since--and this is the
key point-male reproduction is such a quick affair that even
a short life can be adequate to mate with many females.
This looks like a totaJIy pointless system. Everybody seems
to end up worse off. Females are denied the benefits of male
assistance; males, because they have nothing useful to do, are
forced to blow their energies off into the atmosphere and
spend their time fighting with each other. The male striped
bowerbird of New Guinea builds, as his form of sexual adver-
tisement, a display hut. First he selects a plant with a strong
central shoot and strips it down. Then he weaves a thick
column of fibers around the shoot and decorates it with a pro-
fusion of flowers, berries, colorful leaves, and iridescent
beetle wings. Next he builds a two-by-three-foot roof over
the column, leaving a portal through which the column can
be admired, and lays down a lawn of moss in front of the
entrance, scattering red fruit, flowers, and berries over it.
Finally he circles the entire structure with a low wall.
This is a lovely tale, but what is the point? Why devote
so much time and energy to these exotic and sumptuous
love chambers? Is the bowerbird not in danger of being
rendered extinct by some other, more puritan species that will
-put the same time and energy into feeding more young? The
common American grasshopper has a courtship dance with
eighteen separate patterns in it, making it considerably more
complicated than the disco hustle. Why is it necessary?
When one looks at females in nature one sees industry,
The Rule of the Game / 21
theory is closer to Darwin than mainstream evolutionary
thought was twenty years ago.) One key point t~~t should ~e
nderlined is that the theory is explicitly competItIve. Its ~aslc
CHAPTER ~odel is that of a race between two individuals who are m all
respects the same-they have the same genes and live in the
II same environment-except that one has the novel~. and th.e

other doesn't. A Darwinian explanation of an el\lstmg traIt
has been achieved when one has devised a plausible ar~ument
for believing that all else being equal, :reatur~s WIth the
THE RULE novelty will be more fecund than those WIthout It. .
OF THE GAME For example there is a fairly large group. of tropI~al fis~,
called "mouthbreeders," who incubate therr eggs m theIr
mouths after the eggs have been laid-supposedly to protect
them from predators. Sometimes the male i~ the incuba.tor
OVER A HUNDRED YEARS AGO CHARLES DARWIN INVENTED (the mouthbreeders constitute a major fr~ctlO~ of the tmy
the way we now answer questions such as "Why do males percent of fish species [less than 5 perce~tl m whIch the males
exist?" or, for that matter, "Why do fingernails exist?" He contribute some work to the reproductIve cycle) and some-
decided to ignore one part of the question, which was exactly times the female. In the latter cases the female lays the eggs,
why the first male, or first fingernail, appeared-and to takes them into her mouth, and swims off .with them stil~ un-
concentrate instead on why males or fingernails came to be fertilized. The males of at least one specIes of female-m:u-
so common. He just assumed that there is so much noise in the bating mouthbreeders (Hapiochromis burtoni) h~ve eggl.lke
reproductive process that slightly offbeat and novel ways of designs on their anal fins; they also have the habIt of sWIm-
going about life will be continuously and spontaneously ming down to the bottom of the lake and flicking these fin.s.
thrown off. What interested him was the next step; how these Why do they have these designs? And why do they behave m
novelties became standard equipment; how they spread from quite that way? There is one a~ditional fa:t .about these .fish
the very first individual to every member of the species. that instantly suggests a claSSIcally Darwlman explanatlon.
Darwin reasoned that the only way in which a trait could When a female notices a male flicking his fins on the bottom
succeed in thus spreading itself to larger and larger numbers of the lake she immediately swims down to him and opens
would be if it met two conditions. It had to be inheritable, her mouth, 'just as though she were trying to .pick up the eggs
and it had to enhance the fecundity of its bearers. If it met pictured on the fin. What she gets instead IS a mouthful of
these two conditions then it would be passed on to larger sperm. .
- numbers of individuals with each successive generation, until So if one imagines the possession of both the ~gg d~slgns
eventually it became standard equipment. and the knowledge of how to use them to be a smgle mh.er-
That is Darwinism, and in its essentials it has changed itable trait, and one imagines males with this trait competmg
very little since 1859, when The Origin of Species was pub- for females with males that lack it, it seems easy to see why
lished. (In fact in some respects contemporary evolutionary that trait would spread. The males with the designs have hit
upon a trick that allows them to get more females, and there-
22 / WHY MALES EXIST The Rule of the Game / 23
fore produce more progeny, at the expense of the other design- survives, that is well and good, but it does so as the by-product
less males. of a process that only recognizes individuals (or, at. most,
There are two common misunderstandings of evolution that families). Darwinism is surely not the last word ~n this s~b
should be mentioned explicitly. The first is that evolution pro- . ct and no doubt on some issues, at some level, Interspecles
Je , bl
motes survival. This is only indirectly true. What evolution competition is important, but for the purposes of the pro ems
promotes is reproduction. Survival is obviously important to being discussed on these pages, evolution is assumed to b~ a
reproduction, but if and when procreativity is enhanced by a process that goes on between individuals of the same species.
shorter life-span, or by a life-style that necessarily involves So the rule of the game-the game itself is to make some
a shorter life, then early death will be selected. In the last sense out of the existence of males-is that one h~s to i1D;ag- l ,-'1-'''-
chapter there were several examples of males leading risky, ine a non-helpful masculinity evolving by competmg agamst \1 ' 0.'
exhausting, stressful lives that probably killed them much a system in which EVERYONE works to make offspring-and .i~ . r \
sooner than if they had chosen a more serene life-style. winning! Further, because sex is a rela~ionship involving two ,1 ; Co
Nonetheless, given the high levels of male-male competition creatures, a really satisfactory exp~anatlo~ woul.d be one .t~at -I: ".)
that exist in nature, only males that expend their energies in showed how masculinity could Win against thIS competitive ~ .,' \
savage bursts, without counting the cost, can hope to repro- system in two different contest~. The ~rst would s~ow why ~alf :...~;:;'-:
duce at all. Sometimes a shorter life·span might even be the species found it worthwhile to give up making offspnng
selected directly. There are two antipredator strategies gen- and become males; the second contest would explain why
erally adopted by butterfles and moths. One is to secrete the other half of the species, those that stayed female,
poisonous toxins; the other is to look like a poisonous insect tolerated this development. Why did they get into m~e-
but ~ithout actually producing toxins. The genuinely poison: making at all? Assuming that the females had an alternative,
ous Insects tend to have a longer postreproductive life-span so that they could have turned out a full set of off~pring all
than the mimics, who often die immediately after laying their of which were industrious, efficient, and productive, why
eggs. One explanation of this difference is that the poisonous should they have devoted half their output inst.ead to mak~g
insects live longer so as to be available for the education of the creatures that make noise and fight? Accordmg to Darwm
local birds--once they eat the parents, they'll steer clear of there must have been a reason why both those creatures that
the offspring. The mimics, contrariwise, die quickly to pre- became males and those that didn't became better, more
vent the local birds from catching on! Whether or not this is procreative organisms as a result. It is certainly not intuitively
true I do not know, but the example makes the point. Survival obvious why this should be so.
is only important to the degree that it enhances reproduction. Fortunately evolutionary theory also .sug~ests a w~y. to
The second common misunderstanding is that the survival begin untangling these mysteries. If evolutIOn IS a competition,
of the species counts for something in evolution. If so, that then both competitors are equally important to the outcome
fact can't be accounted for by Darwinian theory. Darwinian of the race. Masculinity did not evolve in a vacuum but
evolution always works by, through, and for individuals im- against a specific alternative; perhaps the answer is not th~t
proving their reproductive efficiencies for reasons that have masculinity has anything especially positive to recommend It
to do with their own local circumstances, not because of any -it's just that the alternative is so much worse. There a.re
problems that might face the species as a whole. If the species many species that live without males on the planet, and while
the f~ct th.at they do live genderlessly and/ or sexlessly shows
that In theIr env~onme~ts males are unnecessary, one can still
hope that they ml~ht gl~e some indirect clue as to what might
be the problem WIth trymg to live without males in our world.
CHAPTER
III
LIVING SEXLESSLY
VERY FEW CLASSES OF CREATURES ARE AS RIGIDLY COM-

mitted to a single mode of reproduction as we vertebrates
are. Most organisms (though not most of those we can see
easily) reproduce asexually much of the time, but retain the
option of switching to gene-mixing reproduction once every
ten, or hundred, or thousand generations. In other words, it
is possible to arrange all the forms of life along a sexual spec-
trum according to how frequently they reproduce sexually
as opposed to simply cloning their progeny. If we did this,
warm-blooded vertebrates would be on one extreme and bac-
teria on the other.
Bacteria are the starting point, a reference point, for a good
deal of thinking in biology. They are the smallest class of
creature, and so thinking about the role of size--or lack of it
-naturally centers on them.· They reproduce fastest, are the
most fecund organisms, and so provide a standard of success
that is of special interest to Darwinians. If any life-form can
be called the most successful, important, and best-adapted
on the planet, it can only be bacteria. They are the dominant \
life-form, making up maybe a quarter of the biomass. Prob-
ably 99 percent of all the biological individuals on Earth are
bacterial.
• Viruses are smaller, of course, but for the purposes of this chapter bacteria
and viruses can be treated as a single group.
26 / WHY MALES EXIST Living Sexlessly / 27
Until recently biologists believed that they came only in kingdom has within it a number of members that have been
three shap.es: rods, spirals, and spheres. We now know they continuously viable for billions of years; ~ It has been. hard
can come In any shape: as threads, rings, knots, even as stars. for us to recognize the evolutionary poslhon of bactena be-
There are forms that live without any shape, like amoebas. cause we look at life with a Western, technocratic, chrome-
Some bacteria are the only creatures to have a biological pro- and-tailfins theory of evolution in which evolutionary progress
peller, a real rotor that whirls around, sticking out of their is calculated by the number of different traits and characters
bac~sides. Other bacteria glide like snails over self-generated a species has managed to accumulate. Simplicity, clarity, and \
lubncants; others tether themselves with a ribbon of gum to a economy count for nothing. If it did (and ~erh~ps ~omeday,
s~rface an? then pay it out behind them as they float, like tiny when we devise an Eastern theory of evoluhon, It WIll), then
kItes, out mto the nutrient stream; others root themselves on bacteria would be recognized as the supreme achievement of
rigid stalks, like grains of wheat; while others form vast terrestrial evolution, since which the process has deteriorated X.
colonial fishing nets out of their bodies in which they capture into designing one Rube Goldberg contraption after another. I\,
gases and snare creatures hundreds of times larger than they. The most important feature of the bacterial life-style is its
The largest bacterium is more than a thousand times the size boom-and-bust quality. In general bacterial populations either
of the smallest-a greater range than that between mice and are growing explosively, collapsing catastrophically, ?r lying
whales. They can live and flourish under the most implausible completely dormant. They live like Dionysiac~, wakmg ?nly
extr~me~ of heat, cold, pressure, aridity, salinity, and nutrient when they can live orgiastically, gulping food WIth a techmque
dep~lvahon, and are always the first life-form to appear as that wastes far more than it uses, reproducing riotously, and
enVIronments grow hospitable and the last to vanish. polluting everything about them with their toxins. As soon
They are the most important because every other class of as they have destroyed the conditions that wok~ them up,
living .thing is dependent on dozens of bacterial processes. they just slip away again into dormancy. Bactena are total
Bactena help weather rock to make soil and then stock it hedonists, living only for the short run (and the ~hortest of
with nutrients they produce themselves. All plants, for ex- short runs, at that). And it is this life-style whIch makes
ample, depend entirely on bacteria to process and refine at- possible every one of the scrimp-and-save, puritan, accu-
mospheric nitrogen so that plants can use it. Bacteria form mulating species on Earth.
the first link, or, perhaps better, the anchor, of the food chain. Being small, the way bacteria are, tends to increase de-
(They are the only creatures that could live on an otherwise pendency on local environments. Small creatures generally
sterile planet, .indepe~dently of any other life-form.) And they (compared with larger ones) can cover less ground and must
are the recyclmg engmes of Earth, without whose efforts the find what they need in a smaller area. Their internal volume
nitrogen, carbo~, sulf~r, an~ iron cycles would all collapse. is less, and so they are not as able to store reserves, to build
From an ecologIcal pomt of VIew we vertebrates live like cock- up a bank of nutrients that would allow them to cross, or
roaches and silverfish, in the corners and interstices of a great survive, a depleted environment. In general, they must rely
hou~e built for and maintained by another tenant entirely. more on waiting for the right conditions, all together and at
. Fmally~ they are the best-adapted and most highly evolved
hfe-form 10 the simple sense of having been at it longest. The • Instead of Linnaeus's two-kingdom p1ant-animal system. I use ~ five:
kingdom organization now entering the texts: (1? bactena and vlTuses.
first five-sixths of the history of life, three out of three and a (2) protozoa and algae (the protista) ; (3) fung.; (4) plants; and (5)
half billion years, was given over to bacterial evolution. Their animals.
28 /
WHY MALES EXIST
Living Sexlessly / 29
once, to come to them. This is the strategy pursued by many
forest flowers, for example, which can wait in the form of species can knock out a new generation every thirt~ minutes.
seeds for decades before a tree blows down and a patch of The gene-copying itself is done just the way you mlgh~ ma~e
sunhght appears on the forest floor. Bacteria also have the a copy of a tape recording. Bacterial genes are organIz~d In
knack of waiting patiently, in a low-energy state, often as a long string-usually five to six hu~dred. tim~s the orga~l~m's
spor.es, for the moment when everything is just right for ex- body length-with joined erra5.Thls stnng IS stacked 10 the
plosIve growth. They can endure the most extreme insults cell so that it looks like the cooling coils in the back of a
when .in. this dormant period-boiling, freezing, high levels refrigerator. When it is copied, the whole length rotates, very
~f radIatIon, corrosive chemicals, long periods of time (some- quickly, past a stationary cop~ing head that t?rows off a
tIm.es years)-and still be able to respond to the return of duplicate in the opposite directIon. When bact:na do repro- 1 >({
theIr own kind of conditions. (There is a theory that life was duce sexually, one individual extends a tube IOtO a second
firs.t brought to Earth as an infection by extraterrestrial bac- down which this duplicate gene tape then slides. Some fra:-
terIal spores so long-lived and hardy that they were able to tion of the introduced string-seldom the whole length-IS
sur~ive the journey from another solar system.) It is the then incorporated into the genetic coil of the recipient. (In
arn~al of these conditions that controls the turnover of gen- other words, the bacterium that accepts the genes is funda-
eratIOns; a bacterium might wait weeks or months for some mentally changed by the experience; its genetic identity is
nutrient to appear, duri~g which time it would not reproduce permanently altered. As an example, a bacterium that lacks
at all. When th~t nutnent does appear, it might reproduce
the genes to make a tube and act as a gene donor can
sometimes do so after being mated with. This has led some
ev~r~ twenty mInutes. In human terms this would be like
bacteriologists to say that bacterial sex is a venereal disease,
~altI~g fo: ten thousand years so that everything would be
because it is spread by copulation. Most sexual creatures only
Just nght In order to have one child-and then having hun-
dreds of them. mix their genes at arm's length, off in their progeny, while
~mall ~ize is both an advantage and a disadvantage in com- keeping their own personal gene sets out of the process.)
The important thing about bacterial sex though, is that
petlOg wIth other organisms for a food source. On the one
hand, larger creatures can just brush the smaller aside· on (compared with larger creatures) it is pro~ably very r.are.
Scientists would like it to be more common, slOce many kInds
the ?ther, it takes less material to make a smaller organism.
~ gIven quantity of material makes more little animals than of experiments become possible if bacteria can be persuaded
to mate in a controlled way. Some progress has been made
bIg ones, and little ones don't need to grow as long, or as
in this field, but there are still many kinds of bacteria that
much, to get to their adult, reproductive, weight. So the
no one has succeeded in inducing to mate. Of course what
strategy. that small organisms pursue is rapid, pell-mell re-
productIon. goes on in a test tube may have nothing to do with ,:vents in
the wild. Maybe out there bacteria mate all the tIme; the
As a rule these reproductions are asexual. First an indi-
vidual c~pies its genes and then distributes one copy to each
spread of antibiotic resistance shows that some genes do get
end of Itsel.f. Next it splits across the middle, making two passed around. But most bacteriologists believe that the aver-
( httle b~ctena, which suck up food from the area, fatten to age bacterium is extremely unlikely to have a sex~al expe-
adult SIze, and split again. Under the right conditions some rience. For one thing, bacteria have many adaptatIons that
bacteria can do this every ten minutes, and a great many seem designed to make sure that sex is kept to just a margi?al
role in their lives. Usually just a little bit of the gene stnng
Living Sexlessly / 31
and the other which accepts it. In common
is accepted; the genes that promote transfer are sometimes nates a sex ce11, ak s and ac-
not passed on, and there are other adaptations of the same parlance, males donate sperm; females m e egg
kind. cept sperm. . al
So one could argue that the most successful, important, . . a form of sexual reproduction in which sexu
and highly adapted form of life is also the one that relies on bJSe~aJizi?'ali.ons either do not form or are greatly reducaked
speci . . s can m e
sex the least. Given aJJ the obvious disadvantages of sex-its . . ortance In these specIes the orgamsm
rigidity, complexity, and the riskiness of gene-mixing-this ill ffilP d ggs either at the same time or alternately,
should not be totally unexpected. Surely the minimal infer- ~:cs::e~or: be:both male and female dU:~!~:::
ence one can draw from the fact that a sexless life-form is the life-span. Examples melude many plants .and al
dominant organism on the planet is that doing without sex, Many species of snails and worms are bisexu .
or at most doing with very little, can be a very good thing.
The converse of that observation is that organisms getting
involved with sex are shouldering a burden. We ought not
expect them to do so for frivolous or insubstantial reasons.
At the beginning of this chapter it was remarked that it
( is possible to arrange aJJ the forms of life along a spectrum,
according to how often they reproduce sexually. Bacteria lie
on one end of this spectrum; warm-blooded vertebrates on
the other. In between these two there are a great many or-
ganisms that dabble in both modes. In the next chapter we
will look at some of these, with the hope that catching them
at the moment when they shift into sexual reproduction will
also show us what their reasons for doing so might be.
A GLOSSARY OF REPRODUCTIVE TERMS
sexual reproduction-a reproductive mode in which two or-
ganisms combine their sex cells, creating a set of offspring
in whom the genetic identities of both parents are mixed.
asexual reproduction-the creation by one parent of a set
of offspring that is genetically identical both to the parent,
and to each other. Examples of asexual reproduction in-
clude the splitting of bacteria, or amoebas, the division of
cells in our own bodies, and the reproduction of vines
through creepers. Cloning is asexual reproduction.
gender-a form of sexual reproduction in which the species
divides into two symbiotic specializations--one which do-
An Overview of Some of the Cons and Pros of Sex / 33
able habitats, but alone, will not be able to colonize those
environments.
CHAPTER Finally, since sexual creatures are constantly mixing and
blending their genes from mating to mating, generation to
IV generation, they reproduce themselves only in a general, low-

fidelity, sense. The story is told of a famous actress writing
to George Bernard Shaw and suggesting that they conceive a
child, for, she said, with her beauty and his brains, what
AN OVERVIEW OF a paragon the infant would be! Shaw turned her down, sug-
gesting that their child might as well inherit his beauty and
SOME OF THE the actress's brains. His point was true enough; but neither
CONS AND PROS possibility was anything as likely as that their child would
have had neither, but been much closer to the norm in both
OF SEX respects. As a biological fact, neither Shaw nor the actress
could reproduce themselves except as vague approximations.
This is because humans are sexual animals. Such a behavior
seems completely un-Darwinian. Each parent is already a
winner in the struggle for existence; why should it be selected
ThERE ARE THREE ALTERNATIVES TO WASTEFU to turn its back on the genetic constitution that proved so
males, like beavers or nestin b' d . L MALES: serviceable in its personal experience? Of course the parent
creatures that reproduce ase;u~~1 s, that work; bisexuals; and is mating with another winner, but surely breaking up a gene
three systems is that the 0 . y. ~he key feature of these
. rgamsms In them cl I h complex that has already worked well once and mixing it up
thel~ energies in useful directions. Of them all t~ar y c ann:l with the genes of a second is a real gamble, full of imponder-
cal IS asexuality, or sexlessness i n ' e most radl- ables.
;i~P.IY cloned. Sexlessness is rep;oduc~~~c:it~~urogen[ are Most creatures appear to have found one or another of
der, ~t not only abolishes wasteful males but all ge~e rans- these reasons to avoid sex persuasive, since only a relative
uctIve or not. So the most swee in . rna es, pro- handful engage in it consistently. It appears otherwise to us,
without males is to learn to do P'thgly effective way of doing since if we were to rank all organisms by whether they were
a single parent. WI out sex and reproduce as
readily visible to the unaided eye we would also have sep-
the~:~:gti:!~ {~~~~n sO:::~esat:~mbe~ of ot~er problems at arated the sexual from the asexual, or the drastically less-
ing, is a problematic !nd

energy, takes time requires
trouble:~~~d~u~~~e~:eli;
. .
ene
tmix-
urns up
sexual. As a rough rule, organisms that cannot be seen
-viruses and bacteria, the larger one-celled organisms like
the amoebas, and the smaller multicellulars-reproduce sex-
trouble-free set of h . I a. complIcated and by no means
ually much less often than creatures that can be seen. The
vulnerability. Sex c p ySIO oglca~ ~i?s, and often increases
reason that only a handful of the reproductive events in the
quires a partner th an also be lImiting. If reproduction re-
, en creatures who find themselves in favor- world are sexual is that the smaller creatures are both in-
comparably more numerous and reproduce much more often.
Why organisms reproduce sexually has been argued for
decades. Some believe that sex is an advantage because it
speeds evolution; others, because it slows evolution down,
preventing too tight an adaptation to local, transient circum- CHAPTER
v
stances. A third theory is that sex repairs and rejuvenates
the genes. A fourth theory points out that sexually produced
life-forms have two complete and (usually) different sets of
genes, one from each parent; the virtue of sex is thus the
versatility and resilience that these "backup" genes give. A
fifth idea, and the one relied on here, is that sex is selected THE TRANSITION
when it becomes important for an individual to leave behind
a set of offspring with a wider range of specialized skills, TO SEX
a richer variety of vocational orientations, than she could
possibly make on her own.
Untangling the purpose of sex is obviously not a simple IN MOVING TO THE NEXT STEP, OR STOP, ALONG .THE SE~AL
business, but it has an intimate connection to our subject, trum we cross what many biologists feel IS the smgle
which is males, and how they happen to be here despite their :~~t un~biguous and profound distinctio? that can ~e made
apparent wastefulness. It is striking that (a) we don't under- among living things-that between bactena on one Side ~~
stand what (if any) function males perform; (b) sex makes rotozoa and algae on the other.· All the~e forms are st.1 _
males possible, that is, it was the evolution of sexual repro-
duction that opened the way for the evolution of males; and
~ingle-celled, and to a ~erso~ without af ~Icro~~r~et~:i~;~'
tinctions can mean nothmg, smce none 0 t em b .
(c) the purpose of sexual reproduction is itself somewhat But someone with a microscope wouldn't know how to egm
mysterious. Given two such closely related problems one
might hope that they can explain each other in some way, listing the differences. f h' k' dom
One is that the protists, as the members 0 t IS mg
so that if we really understood sex then we would see the are called are mostly several hundred times larger than ~ac;
point of males as well. Intuitively we all make this connection teria A p~otist that feeds on bacteria, as many do, has a ou
between genders and gene transfer, since we use the word the ~ame relationship to them as does a huma~ to sausa~es
"sex" to apply to both traits. Intuition isn't necessarily right, or french fries. But the most important set of differences m-
of course, but the possibilities it suggests are as good as any volve degrees of internal comptex~ty. In.terna~ or~ans aPfe~
with which to begin. for the first time in the protista, mcludmg digestive an ~x
cretory systems, Most have specialized energy orga?s It at
extract and store energy from the sun or f~om c~elDlca re~
actions They can store materials inside their bodies as welt
fats and starches and excretion deposits. They hav~ attac
and defense mechanisms, including paralyzing secretIOns, ex-
• Well.known examples of protozoa include the amoebas and the paramecia.
36 / WHY MALES EXIST The Transition to Sex / 37
plosive darts, and spines, and powerful propulsive devices, the microflora that live in the gut are ejected with the lining,
which, together with their heavier body mass, allows them so that to the Trichonympha the sudden appearance of the
to swim more smoothly, forcefully, and effectively than bac- molting hormone is the same thing as receiving an eviction
teria ever could.
notice.) First it makes two copies of its genes and distributes
The increase in complexity is echoed (and emphasized) by them to either side, seals itself up into a cyst, and splits ver-
an order-of·magnitude increase in the amount of DNA con- tically into two organisms. So far this is the same procedure
tained in protista genes. Some orders of algae have as much as that followed during asexual reproduction. But this time
DNA as mammals. (It is thought that the way in which evo- when the two progeny squeeze out of the cyst back into the
lution made the "jump" from bacteria to protista was by cockroach gut they are not identical--one is perceptibly
several different kinds of bacteria forming a single, symbiotic smaller than the other. (This smaller one is sometimes called
organization. Over time the members of this association be- the "male" because of its subsequent behavior.) The same
came so harmoniously integrated, their identities as individ- process goes on with all the other Trichonymphae in the in-
uals so commingled, that they evolved into the organs of a sect's gut, and soon the entire tract is pulsing with these
larger order of creature, and so evolved the creature as well.) special, differentiated, progeny. Soon a mass copulation, de-
These larger, more complicated organisms rely on sex scribed by the German zoologist, Wolfgang Wickler, begins:
much more than bacteria do-though they still reproduce
asexually more often than not-and their sex is more thor- . . . the male individual follows the female and penetrates
oughgoing, involving a process by which the entire genetic her from behind through a special zone of plasma. . . . [In the
libraries of both mates get completely shuffled together. (As terms used here, through the bulbous end.] A typical Trichonym-
opposed to just a fragment of the genes, as in bacteria.) That pha female is recognizable by the number of little dark pigment
spots arranged in a dense ring on her rear cell section. The male,
said, we have just about come to an end of all the possible
by contrast, has only a few of these little dots distributed freely
useful generalizations one can make about protista sex. It is
over the entire body of the cell. But there are all manner of
astonishingly various. Perhaps the best one can do is to give
transitions between the two extremes, and one can determine
a few examples that suggest this diversity. how strongly developed the female tendency of such a unicellu-
A first example (anyone of thousands would do as well) lar individual is by the number of dark dots. During a typical
might be the case of Trichonympha (trik-uh-NIMF-uh), a copulation, an individual with only a few dots penetrates one
pear-shaped protozoan that lives in the gut of cockroaches, with a dense ring of dots . . . so it is playing the part of the
where it eats scraps of cellulose. Hundreds of flagella are male. But it will be forced into the female role if it meets up
attached to the narrower part, or head; these drive the crea- with an individual with even fewer dots on its plasma . . . .
ture around by pulling it, breast-stroke style, head-first, In the same way, a rather weakly developed female can act
through the medium. When it finds a piece of cellulose, a as a male when faced by a strongly developed animal. It can
pseudopod reaches out of the more bulbous posterior and even happen that three individuals copulate with one another,
pulls the scrap into the organism. the middle one penetrating the first as a male, while at the same
time serving as female for the third.
Usually a Trichonympha reproduces asexually, by slitting
itself from top to bottom. When it detects the cockroach's Once the two "genders" have come inti:> contact the male
molting hormone, however, it switches to sexual reproduction. gradually works his way into the female's body (or is drawn
(When cockroaches molt they also shed their gut lining. All in, like food) until, bent and cramped, he is completely inside.
T?en he simply dissolves (or is eaten). His cytoplasm merges tive algae pass each other in the water, they br.ing their fla-
wIth that of the female. All that is left of the male is his genes gella into contact. If the two algae are of the nght sort: the
which are drawn upward through the female's body to he; tips fuse and yank the two organisms together. Un~er a mlcr~
"head," where her own genes are stored. There the recombi- scope the algae seem to swim at a terrific velocIty, and t?IS
nation and gene-shuffling characteristic of sex takes place. fusing-and-yanking process, which appears to happ~n In-
Four new gene sets are made, each one of which is drawn off stantly, can look very violent. Once they have been jerke.d
into a different quarter of the super-Trichonympha that was together they both release an enzyme that cuts away theIr
~ade up from the male and female combining together. Then body walls. The "+" cell extends a small projectile tube that
~t (they? she?) divides into four small creatures, thus provid- connects the two and forms a cytoplasmic bridge. The bridge
Ing e~ch set of genes with a cytoplasmic envelope. widens steadily, pulling the two cells together, and a single
ThIS all takes about ten to eleven hours. Meanwhile the "double" cell results. The flagella then unstick and the four-
c.ockroach has proceeded with its molting. The new genera- tailed double organism swims off, probably searching for a
hO~ of sexually produced Trichonymphae are expelled from good place to "hibernate." After a period it (they) forms. a
th.err host and rest dormant in the excreted lining. There they hard spherical coating around itself (themselves) ~d awaits
wIll stay, eventually dying unless another cockroach happens the return of favorable circumstances-usually the nght level
to eat the molt of the first. If that happens, then the sexual of ammonia in the environment. C. reinhardi have lasted in
progeny will start to reproduce asexually until the next evic- this condition for at least four years. When it does detect the
tion notice is posted. right conditions the alga shuffles its genes and divide.s itself
A slightly different example of sex among the protista is into four progeny among whom all the cellular protems ~re
that of a small alga, about the size of a red blood cell, called distributed. The spore hatches and the four small algae sWIm
Chlamydomonas reinhardi (c1am-a-da-MoN-as). This is one away. The parents are not quite dead, since in a sense they
of those creatures that made problems for the taxonomists have transformed themselves into their four progeny; and
working under the old two-kingdom, plant-or-animal c1assifi- they are not quite stilI alive, since the sexual process has made
~ation, since it ~oth carries chlorophyll and is mobile, driving their progeny genetically distinct from their parents.
Itself toward lIght sources with two "arms": strong, long These two examples of protist reproduction show that the
flagella that pull it forward breast-stroke style. All it needs switch to sex is often associated with the destruction or col-
to support itself are sunlight, water, some dissolved salts, and lapse of the habitat in which the asexual r~production we?t
a steady supply of nitrogen which it gets from ammonia in on. Microbiologists find that often they can mduce sex at WIll
the water. When those resources are all available it reproduces in laboratory cultures by letting, or making, condition.s d:-
asexually, splitting from top to bottom every eight to ten teriorate: by lowering the culture's temperature, or let~g It
hours. dry out or by withdrawing vitamins or some other nutnent.
The algae only switch to sex when the supply of ammonia On the ~ther hand sex can be forestalled, often seemingly for-
is exhausted, or withdrawn by a meddlesome experimenter. ever, by tenderly ministering to the organism's needs. The
There are two genders (though microbiologists do not call changes that induce sex would, in the real world, be events
them male and female, but, somewhat more neutrally "+" like the coming of winter, the evaporation of a pond or pud-
and "-"). All matings involve one of each. When two ;ecep- dle, the exhaustion of a nonrenewable nutrient-changes that
would be catastrophic and irreversible. From a distance pro- palintomy. These terms at least show what a supermarket of
~ist sex often looks literally like a last fling, something engaged prefixes, roots, and suffixes are needed to label the strange
In by the last generation to live in a habitat that has supported varieties of protist reproduction.
that population for many generations.
Continuing to move along the sexual spectrum brings us
That point is relevant to the inquiry at hand, but it is really over another dividing line, that separating the single-celled
~ot what is most interesting about protist reproduction, which from the multi celled creatures. Many of the larger multicelled
IS the overwhelming variety of it all. Two examples do not
organisms are committed to sexuality. There are very few
begin to do justice to their zany imagination. Many reproduce asexual amphibians, reptiles, or fish; no known asexual mol-
by mutual immersion, like Trichonympha; others, less head- lusks, which is a huge group of species comprising all shell-
long, form a cytoplasmic bridge between the two individuals, fish, snails, squid, and octopuses. There are no asexual birds
over which the gene copies migrate. Usually this exchange is or asexual mammals (the instance recorded in the New Testa-
reciprocal, with two gene copies passing each other over the ment is thought to be unique).
bridge, but sometimes it is just one-way. Then the participants But some of the smaller multicellulars still retain the
~eparate and continue an independent life. Sometimes they asexual option; one of these is a powerful little protist preda-
Incorporate the new genes into their own functioning set, the tor called a roti/er. While these animals are still too small to
way some bacteria do, and in other cases they hold the new be seen easily, they represent another big "advance" in com-
s.et in storage until the time comes to make offspring. Some- plexity over the protista. In general they are squat, chunky
lImes two Paramecia will undergo all the preparations for creatures that look a little-a very little-like those small,
mating-meeting, aligning, joining their surfaces, building a tubular, electric coffee grinders, but with their blades exposed.
bridge, making a copy of their genes-<>nly to stop just short Most rotifers have hard, pointed jaws that can sometimes
of the actual migration itself. They then destroy the original be extended to grasp and chop into their prey. They often
gene sets and recreate their nuclei from the copies. Thus the have body armor in a wide variety of shapes and types. They
interaction, ostensibly for mating purposes, was really a way have a brain, a complicated chewing apparatus, muscles, di-
of mutually stimulating each other into a genetic houseclean- gestive glands, a nervous system, a urinary bladder, and,
ing of some kind.
sometimes, a foot with two toes that they use to help them-
Asexual and sexual reproduction can be combined in many selves move over certain surfaces, humping along inch-
ways. There is one protozoan (Polyspira) that lives in the wormlike. Some rotifers are even capable of major bodily
molted skin of hermit crabs. Individuals first join into pairs alterations. There is one species (a Brachionis) that is normally
(called syzygies) which look vaguely like yin-yang symbols. spineless. In this vulnerable condition it can find itself being
Then they split, asexually, again and again, each time re- hunted by a second species of rotifer. If the predator rotifer is
ducing their volume by half, until they end as a chain of six introduced into water samples containing the prey, the next
~r eight pairs of much smaller yin-yang symbols, arranged generation of the Brachionis to appear will have spines; the
lIke beads on a string. Only when this division has stopped length of the spines will depend in part on the number of pre-
does the sexual exchange take place between members of the dators in the parents' environment.
small pairs. Then all the individuals split up and disperse. Like the single-celled protists, rotifers seem to prefer to
Some biologists call this syndesmogamy; others call it zYgo- reproduce asexually. Females lay unfertilized eggs that hatch
into more females. In some cases, however, some species of populations multiplying like this have reached 20,000 per
rotifers can be induced to make males and reproduce sexu- square foot in five weeks.
ally. These males are usually dwarfed and highly simplified That is the asexual phase. * There is also a sexual form,
(their digestive systems never develop), and have life-spans which is winged and egg-laying (the young develop outside
of not more than a few hours. They are adapted to find and the mother). And just as with the rotifers, there are two kinds
fertilize a female--quickly; nothing more. A female making of effects that trigger the development of this sexual form:
these little males will continue doing so until she is mated starvation and crowding.
herself (not necessarily by one of her own progeny, of course). As one continues to move along the sexual spectrum, two
She will then switch back into making females again; the only observations stand out. The more sexual a creature is the
difference is that her next clutch of daughters will hatch from larger it is (and the more long-lived and physiologically
fertilized eggs. complicated), and the more likely it is to live in an environ-
One way of inducing sex in rotifers is by letting the environment that is crowded with members of the same species over
ment deteriorate (by starving them, for instance); this is the the long run. Asexual marine organisms are more likely to
same "last-fling" effect noticed with the protists. John Gilbert, be found in the ocean depths than in the biotically richer,
a zoologist at Dartmouth, has found that rotifers will also more crowded, surface. (Similarly, there is a European flat-
switch to sex when they are crowded into dense populations. worm [Pianaria aipina] that is sexual when it lives in rich,
.
Crowding them with protists does not have the same effect·,
.. warm climates but reproduces asexually in Scandinavia.)
It has to be with numbers of their own kind. Gilbert points Asexual sea anemones tend to live in shallow water, where
out that male rotifers are more often found in nature at high temperature, salinity, and degree of exposure to the sun's rays
population densities as well. He believes that they census all vary greatly; these pools may get crowded from time to
their populations by monitoring the concentration of a chemi- time, but only over the short run. The sexual anemones live
cal they release into the water. 2 • lower down in the intertidal zone, where the pools are deeper
Other multicellulars show these same two associations with and more stable conditions promote a more extended com-
the switch to sex (crowding and habitat collapse). The gall petition. The few known asexual vertebrates seem to be almost
midges are tiny flies that feed on mushrooms and other fungal all animals that specialize in temporary habitats created by
growths. When this fly finds a mushroom-such a food source fire, flood, drought, or tree blowdowns. Most of the asexual
might be hundreds of thousands of times its size-it will mul- lizards, for example, are found either along the edges of
tiply, asexually, at a breakneck pace. It does this by drastically
reducing the time needed to reach a reproductive state. The • This principle of beginning to reproduce white stilt a juvenile and doing
young of each succeeding generation grow inside the mother, so by converting one's internal tissues into o~sprjng. is also ~ollowed by the
best·known asexual insect, the aphid. In this case embryoOlc development
so tha.t, ~s she eats on the mushroom, her young eat her up begins in aphid mothers before they themselves have e~en been born, so .th~t
from insIde. (A more accurate way of putting it might be jf one looks at the right time one can see two generations telescoped wlthm
to say that she transforms herself into her young from the a single aphid grandmother-to-be. It has heeD calc~lated that .i~ one of, the~
species a single individual can transform herse~ mtc 524 b~lh0!1 a~hlds In
inside out.) By the time the larvae emerge, the mother has a single year. Aphids also have a sexual, egg-Jaymg .form which IS tnggere~,
been reduced to a hollow shell, and within two days, the next at least in those species that live in temperate lahtud~, by a d~crease l!,-
the length of the day. They then mate and lay eggs which overwmter until
generation will be consuming the larvae in tum. Gall-midge the spring.
44 / WHY MALES EXIST The Transition /0 Sex I 45
forests, or where trees have been disturbed or destroyed, or leave 20 cubs; a pigeon, 150 chicks; a mouse, 1,000 kits; a
in the floodplains of rivers, streams, and washes. A number trout, 20,000 fry, a tuna or a cod, a million fry or more; an
of these species are known in the American Southwest, where elm tree, several million seeds; and an oyster, per~aps a hun-
the rough terrain, sparse vegetation, and extremely uneven dred million spat. If one assumes that the populatIOn of each
precipitation make flash floods particularly destructive--es- of these species is, from generation to generation, roughly
pecially to something as small and vulnerable as a lizard. It equal then on the average only one offspring will survive to
has been speculated that construction in the Rio Grande Basin repla~e each parent. All the other thousands and millions will
has, since 1941, so effectively controlled flooding that a num- die , one way or another. This "excess" fecundity .. can. be
ber of asexual populations have been wiped out. pruned back in only two ways. One is by co.mpetltlve I~ter-
As was mentioned briefly in the last chapter, the theory of actions with other members of the same specIes (by whIch I
sex these pages rely upon is that sex is selected when and as do not mean fighting so much as another member's getting to
it becomes important for an individual to have a diversified set a needed resource first, though of course direct, physical
of offspring. An asexual organism can only reproduce itself; competition counts too). The second way is through fluctua-
if it has specializations, all its progeny will have to pursue tions in the ecology, the depredations of predators and para-
the same trade, practise the same tricks. But a sexual crea- sites, and, in general, the influence of natural forces. or
ture, by joining its genes with another organism (and at the creatures that are very different from the affected orgamsm.
next mating go-around with a third, and then a fourth), ex- The first type of species controls its own population growth;
pands the range of vocational orientations that are passed on the second depends on nature to do it. To put it another way,
to its offspring. To put it another way, sex ought to be selected all living things are victimized either by nature or by ~ociet~,
as it becomes more important to a parent to have offspring and they are all victimized to the same degree, until theIr
that are distinct individuals, different from their siblings alld populations have been cut back to replaceme~t lev~l.
their parents. Most biologists believe that the larger an ammalls the more
If this theory is right, then questions about the role of sex important social competition is likely to be i.n tha~ ~peci~s'
transform into questions about the importance of specializa- scheme of population control. One way of argumg thIS IS qUIte
tion and individuation. Judging from the evidence in hand so indirect; it says that larger animals are inherently better at
far, across all species as a whole, there should be some reason coping with ecological fluctuations, because if an unpleasant
why individualism becomes more important as species get situation comes up they can physically remove themselves to
larger, live longer, and as they live in more stable and crowded search for a more pleasant one. They have more powerful
environments; while, within just those species that can switch swimming surfaces (or legs), more bodily mass with which
modes freely, having varied progeny would become important to retain heat and conserve momentum, and more internal
when a habitat is about to collapse, or when it gets crowded. volume for reserves and stores and specialized organs. Since
In trying to spell out why these links should exist I have excess population has to be trimmed back either by nature or
found it helpful to imagine a second way of comparing all by society, therefore large creatures must be relatively more
species against each other (in addition to the sexual spec- vulnerable to social competition. Or one can argue that large
trum). This might be called the means-of-population-control creatures are more likely to run across each other and influ-
spectrum. All species reproduce to excess, way past the carry- ence each other's fortunes. In fact size itself is thought some-
ing capacity of their niche. In her lifetime a lioness might times to be an adaptation to social competition, since a good
The Transition to Sex I 47
big guy, as the proverb goes, will always beat a good little guy. the same resources, can make for each other. (Bacteria-type
To return to a point made earlier, the world that small organisms do not have these problems, by contrast, because
creatures, those with boom-and-bust population cycles, live by the time resources get short enough to be fought over the
in is a uniform one. It has only two states: abounding plenty whole habitat has become unendurable.) What kind of adapta-
and unrelieved famine, and the latter replaces the former in tion will be selected by socially competitive creatures living
a blink. The reason is that in populations with soaring in a multitextured world?
growth rates every generation but the very last one, the one The answer is obvious: individual specialization. One sees
for which everything comes to an end, enjoys abundance. the same result looking at human society. Specialization has
If the population doubles with each generation, the parents gone much further in stable, crowded, enduring, competitive
of the last one of all will, as they start to breed, gaze out societies (like New York!) than in either boom-and-bust
contentedly on a world that still holds as yet unexploited a populations (like the crowd in a stadium) or in less crowd:d,
full 50 percent of all the resources it has ever contained. rural, areas. Theoretically specializations in nature can Ill-
(This point is sometimes made to those who believe that volve a concentration on any feature of the life-style: being
the existence of large oil reserves undercuts the claim that specially skilled at finding one kind of item in a species' diet
there is an energy crisis.) Ecologically organisms on the range rather than another, or being extracompetent .at c~n
bacterial end of the scale live in a world that is almost al- verting certain foods into cellular materials. One can lmagllle
ways lush and ample and rich. When the niche closes up-- specializing in certain specific foraging styles. Some me~bers
perhaps a bigger competitor has arrived, or the population/ of a species might be good at being bold and aggresSIVely
resources ratio becomes impossibly unbalanced, or the accu- pursuing suggestive possibilities, while others might be good
mulation of wastes reaches toxic levels-it does so quickly, at being cautious, and steady, and sticking to the well known.
for everyone at the same time. The organisms all flip into Another fraction of the population might be professionals at
dormancy, into seeds and spores and other low-energy states. stubbornly coping with a slowly deteriorating environment,
(It is while they are seeds or spores, for the most part, that while others may be expert at how best to search for a new
their numbers are cut back; more often than not, the favorable one. Some may forage best when and where the food is rich
environment they need does not return until even the seed's but the number of competitors high; others where the country
formidable powers of endurance have been exhausted.) Fi- is poorer but the social circumstances are more relaxed.
nally, their world is socially very uniform as well. They are sur- So the theory is that specializations are defined and pursued
rounded by members of the same clone, asexually produced, when a socially competitive species lives in a world with some
genetically identical siblings, and all these siblings are doing variety to it. Is there any direct evidence for this theory?
just two things-gobbling and splitting, gobbling and splitting, Some, but, unfortunately, not much. It is hard to get firsthand
over and over, as fast as possible. observational evidence on this subject-to figure out what the
By comparison, large creatures, which live in, forage over, professional structure of a species might be-because all the
and grow through a succession of diverse environments live members of a species (usually) look the same, regardless of
. '
III a world with a rich texture of problems and possibilities. what speciaJization they might or might not be following.
At the same time they are being pressed by the forces of social They have no distinctive occupational titles or cues. If they
competition, which refers to the problems that a population did it would be possible to associate differences in the way
of interacting organisms, all with the same needs and after two animals live with differences in their labels and maybe
WHY MALES EXIST The Transition to Sex / 49
48 /
draw some conclusions from that. Evidence like this is much The flies are then allowed to breed for a number of genera-
easier to get by looking at what happens among individuals of tions; with each generation the proportion of the whole pop-
different species, because they do look different. Here we do ulation made up by each variety is recorded. Usually these
see this principle-that competition forces specialization- proportions vary dramatically: Variety A might be dominant
confirmed; in fact, the confirmation is so powerful that it is for a while, then B, and then A again, and then C, and so on.
practically a law, and is stated thus: No two species can exist These fluctuations are believed to reflect the changing propor-
at the same locality if they have identical ecological require- tions of the different foods on which each variety has special-
ments. This is called the exclllsion principle, and it is based ized. Variety A will be dominant for a few generations because
on the belief that if two species try to live in the same way its preferred food happened to be most abundant when the ex-
at the same place, one, by virtue of slightly superior specializa- periment began, but, as its numbers multiply and the amount
tion to the conditions at hand, will always exclude the other. of that kind of food declines, a point is reached when the food
There are many famous examples of this principle; one of on which B specializes becomes more common and B becomes
the best-known is that of the fauna that live on cow dung. One dominant.
study showed that of fifty-one different species of nematodes These specializations need not always have to do with
(worms) that were found to eat bacteria and fungi in cow foraging. Pine trees can be infested by little parasites called
dung, none seemed to be in direct, head-to-head competition. scale insects. Botanists have reported that the intensity of
All had their own specialization, their own trade. Some lived infestation by these insects varies enormously from one pine
on the surface, others at different depths of the interior, or to another. One report notes:
at different stages of decomposition, or different levels of Scale-free pines frequently stand for years beside trees infested
moisture, and so on. Arguably if anyone of those fifty-one with as many as ten insects per centimeter of needle, often with
species were to find itself in sole possession of a piece of cow intertwining branches. Scale-free trees tend to remain unin-
dung, then it could manage, however clumsily, to forage over fested even though . . . larvae can be seen crawling on their
a much wider range of conditions than it does now. But the needles during the insect's reproductive period in July. When
competition of the other specialists forces it to stick to what plots of trees are sprayed with insecticide to control the scales,
trees are reinfested ... to approximately their original level
it does best. A jack-of-all-trades-but-master-of-none nematode
of infestation; that is, formerly severely reinfested trees become
that wandered vaguely about trying one thing here and an- severely reinfested, previously lightly infested trees become
other there, could only sustain so inefficient a foraging style
lightly infested ...""
if its cow dung was lush and rank and overgrown. In real life
the average piece of cow dung is harvested much too metic- Apparently individual trees differ in which kind of anti-
ulously by the specialists for it ever to lapse into so abandoned insect toxin they produce, while the insects differ among
a condition. The theory being used here says that competition themselves as to which toxin they can neutralize. The trees
within a species has the same effect. Specialists emerge, divvy have not been able to evolve a toxin that will protect against
up the territory, and drive out the generalists. every scale; the scales have been unable to devise a neutralizer
Nonetheless, for all the difficulties, there is some direct evi- that will render all the toxin varieties harmless. Instead of
dence on intraspecific specialization. There is a common ex- either one of these solutions we have two armies of specialists
periment with fruit flies in which different varieties of the parrying with each other.
same species are placed together in a cage with a mix of foods. Occasionally one finds species in which the specialists are
visibly different, though such finds are rare. Recently a group offspring like that would be outcompeted at everything they
of Mexican fish (Cichlasoma) that were thought to be com- tried. Nor is turning out just one kind of specialist a good idea.
prised of several different species were reexamined and identi- In the first place, all her offspring will be competing against
fied as a single species. These varieties differ in tooth structure, each other, but, more importantly, the parent would be putting
body shape, gut length, and diet. One variety eats snails and all her eggs in one basket. Who can tell where the oppor-
has teeth adapted for crushing shells; a second eats algae; and tunities are going to lie by the time her progeny have grown
a third eats other fish. The single-species identification was up? Far better to cover her bets, produce a mix o~ ~pecia!i~ts,
made on the basis of genetic analysis and the observation that and so position herself to profit from opportumtles ansmg
these three varieties were found being raised in a common anywhere on the vocational spectrum. And the technique that
brood.'" turns that trick is sexual reproduction.
It cannot be emphasized strongly enough that all the issues Sex therefore is a social adaptation, springing from and
of specialization are social issues. The argument has already responding to social dynamics at every point. It follows nat-
been made that specializations themselves only evolve when urally why it should be associated with stable, crowded .popu-
there exists a society of interacting competitors. But even lations. The correlation with habitats poised on the brmk of
when specializations have defined themselves, whether or not dissolution is less obvious. It may be that these small, mostly
they work for the organism will depend solely on what everyone-celled parents compete over who is going to get the first
one else in the species is doing. Specifically, the more indi- jump over the others when the next good environment ap-
viduals there are in a given vocation the worse life will be for pears. The first algae, say, to begin reproducing asexually in
those specializations. The more flies there are in Variety A, a new habitat has a good chance of multiplying so fast that it
comparatively, the rosier prospects will be for the Variety B can take over much of the puddle all by itself, so that the
flies, since they will have fewer competitors in their specializa- habitat is filled just with descendants of one or two designs.
tion. The fewer neighbors that a pine tree has that mount the An alga spore with no competition would take its own
same anti-insect defense that it does, tlie better; otherwise, sweet time about waking up and beginning to swim and split;
if one of those neighbors' defenses is penetrated by an insect, it would wait until it was absolutely sure that good conditions
then that pine tree will be caught as well (by that insect's had in fact appeared. But a spore with competition does not
progeny). It is far better for a tree to be the only specialist of have this luxury; it must guess and run the risk of opening
its kind in a grove. (The same point can be made about prematurely. A parent might then be expected to build a range
gender specializations. The fewer males there are the better of progeny, some impetuous and daring, others temperate and
it is to be one, and the more, the worse.) , judicious, still others very conservative and extremely slow to
In other words being a specialist is not necessarily a good test the waters. The only reason it diversifies its offspring like
thing; if an organism has too many fellow-practitioners in its this-an act which insures that most of its progeny are going
specialty it might end up even worse off than if it had been to be inappropriate for whatever environment does appear-
a. g:ne~alist. At least generalists have some flexibility; a spe- is because all the other local parents are doing the same thing.
CialIst I~. a c~owded profession is condemned to a frantically When these smaller organisms reproduce sexually, they are
competitive lIfe by the very rigidity of its specialization. positioning themselves to deal with one of the few moments
Faced with all these considerations, what's a parent to do? in their lives when the society of others of their kind is im-
She can't make a single, all-purpose model progeny, because portant to them, and that is the scramble to be first over the
t~reshol~ into a new environment. The rest of the time they
lIve asoclally, and therefore asexually.
~o, the the?r~ of sex is that social competition selects a
s?clet~ ~f speCIalIsts, and specializations themselves select sex
smce It. 15 advantageous for a parent to breed a little societ; CHAPTER
of speCIalIsts herself. The critical idea of this chapter the on
t~~t has the most importance for the chapters to foll;w is th:
VISIOn of s.exual societies being composed of interacting' guilds
?f professIOnals. And at the core of that idea should be the
ll~a~e Of. ea~h. member of these civilizations being highly spe-
VI
CIalIzed, mdlVldualized, and competing by being good at what THE CONSEQUENCES
he or she does-by harvesting efficiently and skiIIfully_ OF BEING SEXUAL
rather than through physical confrontation.
IN THE LAST CENTURY A FAMILY OF MARINE JELLYFISH

called the Siphonophora (the man-of-war is one) became
involved in nineteenth-century socialist thought. Naturalists
studying these animals showed that each jellyfish was really a
tightly coordinated ensemble of several separate individuals,
all working toward the common good. Every one of these
"component" individuals had its own nervous system, digested
its own food (which was delivered to it through a communal
pipeline), and often had other features of self-sufficiency,
depending on the species. But each "individual" also worked
cooperatively with the others. For example, one might form
a balloon that kept the whole colony afloat and drive it before
the wind; a second might pump water to propel the colony;
a third might prepare the material to be delivered down the
communal pipeline; a fourth might form tentacles and look
out for the defense of the colony and the capture of prey; and
a fifth might occupy itself with making the colony's next
generation. The socialist community seized on this phenome-
non as a parable of the utopian state. "As in a communist
state," one lecture ran, "there are here no poor by the side
of the rich, no hunger beside surfeit, . . . no lazy next to
the industrious. Each one contributes his part to the existence
and welfare of the whole. . . ."
54 I WHY MALES EXIST The Consequences of Being Sexual I 55
What the Siphonophora teach us is that there is more than alarmone are also released; this prevents the "noise" of back-
one way to be a specialist; it is perfectly possible to be a wash eddies of the hormone from distracting the congregating
specialized member of a large organization. But sexual crea- amoebas. Only a direct pulse is large enough to override the
tures tend not to be this kind of specialist; they are generally effects of this "muffling" enzyme.
II free-living, independent, self-sufficient individuals. "Sex is an
antisocial force in evolution," E. O . Wilson says flatly in his
As the ripples of alarmone spread out through the neigh-
borhood hundreds, and then thousands, and finally tens of
magisterial book, Sociobiology, by which he means that thousands of amoebas converge on the first sender. They line
tightly integrated organizations tend not to be made up of up in circling streams that spiral in on the point of aggregation
sexual organisms. The Siphonophora have a sexual stage, or like the arms of a whirlpool; each time a ripple sweeps out-
state, but it is not a colonial individual. When sex cells made ward all the amoebas affected by that wave take one "step"
by two Siphonophores of the right species join, they form a inward, amplify and relay the ripple outward, and then rest.
solitary, single-celled "seeker" that swims about looking for Moving amoebas appear brighter than resting ones, so that
the right time and place to begin a colony. Then it buds off under a microscope and with the right kind of illumination
asexually all the cells that make up the colony, so that each one sees concentric, alternating bands of light and shadow
colonial cell is genetically identical. encircling the center. As time goes on-this whole process
A second test of organized solidarity (besides a collective takes eight to ten hours-the pulses of alarm one come faster
of specialists) is altruistic sacrifice-the laying down of one's and faster. The dark bands, indicating resting amoebas, shrink
life so that others might live. A dramatic example of this- steadily, and the whole joustling throng seems to be in con-
one that would delight the German socialists as much as the tinuous motion. As the amoebas aggregate they pile up in the
story of the Siphonophora-is that of a social fungi (Diet yo- center, forming a tiny, upright, fingerlike body. Somehow the
stelium discoideum) called the slime mold. Part of its life it colony as a whole senses how big it is getting, because when
lives as a free-living, independent, amoeboid individual, roam- it has recruited about one hundred thousand cells, and grown
ing through the debris of hardwood forests, foraging on the to about one-twenty-fifth of an inch long, the finger topples
bacteria that in turn feed on decaying wood. These cells over on its side. The slug orients on a source of heat and
split, reproducing asexually, every three or four hours, multi- light and begins to crawl toward it. It does this by comparing
plying at this brisk pace until the population of bacteria has the amount of energy received on its front end with the
sunk to very low levels. At this point one or two of the amount received on its back end and directing itself so that
amoebas in the area begin making and transmitting pulses of the front end always receives more. (The slug can perform
a certain hormone. This hormone (sometimes called the these calculations with such uncanny accuracy that it will
alarmone because it is involved in starvation reactions in a orient and crawl toward a spot of fluorescent paint dabbed on
great many species, including humans) spreads out in circular a laboratory wall.) In nature this behavior will bring it out
ripples. When it hits other amoebas something about the from under dirt and leaves into the open. A slug is capable
angle of the ripple-body contact tells the receiving amoebas of pursuing an energy source, at least in the lab, for as long as
where the sender is, and they begin to crawl in that direction. ten days.
~t the same time each receiver puts out a pulse of alarmone When the colony senses that its energy source is overhead,
I~elf; this pul~e is timed such that it will fall into synchrony it reshapes itself into a Mexican-hatlike form . Eighty percent
With the first npple. Small amounts of a chemical that destroys of the slug's component cells change into hard, dry, resistant
The Consequences of Being Sexual / 57
workers are busy carrying them back again. StiU other workers
spores. The remaining 20 percent elongate themselves verti-
run back and forth carrying nothing. . .
cally, boosting the spores up into the air, as though a glassy
lemon were being lifted by a rapidly extending fiber-glass rod. Obviously the image of an anthill as a tightly regim.ented \
These stalk cells form a tough, cellulose scaffolding around society in which, to use T. H. White's phrase, all that IS not
their outsides and then die. The spores contained in the head mandatory is forbidden, is exaggerated. Much ~an be acc~m
wait to be swept off by wind or water to more fruitful con- plished by these inefficient, freewheebng, quasl-democracl~s,
ditions. The twenty thousand cells that made up the stalk of course, but they are simply not in the same league for dIS-
have died so that the other eighty thousand can have another ciplined and elaborate organization that the asexual c~lIs ?f
turn in their life cycle. What better example could one have our bodies are. We have dozens of specialist castes (which ID
of a noble, self-sacrificing, generous devotion to the common our case we call specialized tissues), not just t~o ?r three.
good? But even as comparatively simple an orgamzatlon as a \
Stories like this involving sexual creatures are hard to come colony of social insects has found it ne~ess~ry to suppress se~ .
by. One can't say flatly that sexual organisms never sacrifice Eleven of the twelve families of SOCial IDsects make their \\
D themselves to the interests of others, and never form orga- males asexually. When the queen lays an egg she can choose
whether or not to withdraw a sperm from the sper~ bank
o nizations of mutually dependent specialists. There are excep-
tions, but in most cases even these seem to have made a she received when she was fertilized. If she does fe".lbze the
special effort to sidestep the influence of sex. One such set egg with a sperm, then the egg becomes a female; If not, a
of exceptions are the social insects-the social bees, ants, male. Males, in other words, have no fathers, only mothers;
and termites. Colonies of these insects usually are composed females have both.
of two or three different castes, or specialists; the altruism of Because the males have no fathers they inherit only one
these workers, their willingness to fling away their lives in set of genes, their mother's. And when they get around to
defense of the colony, is famous; and such nests typically making their sperm they have just this one set t? ~raw from.
depend on the efforts of castes of workers that, while techni- With only one set of genes there can be no vanatlon among
cally female, never lay eggs of their own. (From a Darwinian their sperm-all the sex cells any individual male makes dur-
point of view this is just as self-sacrificing as a bee worker ing his short life will be identical. (By con.trast, a sexually
plunging her stinger irretrievably into someone she sees as a produced male, like a human, would bUild hiS sperm by mix-
threat. ) ing together his mother's and his fat~er:s gene~; almost cer-
These insect colonies are wonderful entities, but one can tainly each time he does this a quabtatlvely different sperm
exaggerate how organized they are. E. O. Wilson writes: will result.) When that male mates with a queen-to·be, .he
leaves her with a large number of identical sperm, all of which
An important first rule concerning mass action is that it usually she stores in her sperm bank. The queen uses t~ese sperm .to
results from the conflicting actions of many workers. The in- make daughters. The result is that the females ID most SOCial
dividual workers pay only limited attention to the behavior of
insect colonies resemble each other much more closely than
nest-mates near them, and they are largely unaware of the
moment-by-moment condition of the colony as a whole. Anyone sexually produced sisters usually do; as far as the ge~es t~ey
who has watched an ant colony emigrating from one nest site got from their father are concerned, they are all Identtcal
to another has seen this principle vividly illustrated. As workers twins. . )
stream outward carrying eggs, larvae, and pupae . . . other The reason that social insects (eleven out of twelve ttmes
58 /
WHY MALES EXIST
have found it necessary to suppress sex is probably that indi-
viduality is a problem for any organization. Members of an even come close to the tight, intimate, mutual depende~cies
\ organization are interdependent; there is a general reliance that we see in such classic symbioses as that of the fungI. and
on all members routinely discharging their particular duties. algae to make lichens, or that of the clovers. ~nd bacterIa. to
Since sexuality seems intimately involved with the thorough fix nitrogen (make natural nitrogenous fertIlizers). The 10- \
distribution of individual differences in a population, it is easy stitution of the community specialist that we .saw so well
to see why it might be suppressed or never allowed to appear exemplified in the jellyfish Siphonophora, wherem o~e mem-
in an organization. ber concentrates all its energies on one phase of the life cycl.e
.Sex~al creatures do often pool their efforts by flocking, while being completely dependent on others to support It
mlgratmg, and/ or breeding together; combining their powers through the other phases, is virtually absent among se~ual
of observation and/ or resistance makes them all safer. A organisms. By and large associations among sexual orgamsms \ \
nineteenth-century biologist, Francis Galton, put the matter form when it becomes profitable to pursue, as a flock or herd
thus: or group, the same sorts of activities that each one would be
doing if it were alone. .
I To live gregariously is to become a fibre in a vast sentient
web overspreading many acres; it is to become the possessor of
Typically the members of a group of sexual ammals com-
pete among each other on some issues while they coop~rate
faculties always awake, of eyes that see in all directions, of ears on others. A good example of this :-vas f~und recently 10 a
and nostrils that explore a broad belt of air; it is to become the
study of communally nesting birds, 10 whIch more than o~e
occupier of every bit of vantage ground whence the approach of
a lurking enemy might be overlooked. . . . mated pair join forces in a singl: !arge nest. These pal~s
cooperate to guard their young Jomtly; ~hey b:ood thetr
It has been suggested that little fish combine into a school eggs and feed the fledglings with no Ob~lOUS bIas to~ard
so as to disguise themselves as a single giant fish, large enough their own offspring. Darwin, and others smce, have notIced
to be their predator's predator, and so scare him away. A that such nests often have eggs strewn about th:m. Explana-
second explanation of the point of cooperative assemblies is tions for this waste usually invoke a presumed fatl~re of s.ome
'( that When prey animals cluster they become harder to find, kind in the breeding system; Darwin himself attrIbuted It to
because they are dispersed less evenly in space and time. male incompetence at brooding. Recently Sand~a Vehrenca~p
Predators have to spend more time searching or waiting for of the University of California investigated thIS egg wast~ 10
them; this inconvenience reduces the number of predators and one such species, the groove-billed ani (Crotophaga su/clro-
therefore, the number of attacks that the flocking animals stris) , in Costa Rica. .
must suffer. Galton's point-that flocking animals profit from Vehrencamp found that the females were roll~ng ~ac~
combining their powers of observation_is still widely cited. other's eggs out of the nest! She believes that there IS a lImIt
1
Flocking also seems to be the best strategy to pursue when to the number of nestlings that any group can brood, fe~d,
harvesting a wide range of foods. and defend, and that females compete within the coop~ratIve
The point to be made here is that sexual members of these framework of the communal nest to see who can .acquIre the
associations keep strict limits on the degree of dependency largest share of these "nestling sl?ts". ~ female ~ill only roll
they allow to spring up between them and the rest of the flock. eggs out of the nest until she begms laymg herself, apparently
Symbioses among sexual members of the same species do not (and incredibly) a female cannot tell her. own egg~ from
those laid by other females, so to avoid the rIsk of tossmg out
60 / WHY MALES EXIST The Consequences of Being Sexual / 61
her own by mistake she then stops rolling them out altogether. selves into the stalk. Yet those cells' sacrifice is really no dif-
Therefore, early-laying females lose more eggs than late- ferent than that of mothers; since the slime-mold amoebas
laying females. The female to lay last loses none, and stands reproduce asexually, all the organisms likely to congregate
to garner the largest proportion of nestling slots for her own into a single slug are identical to each other. In a sense, there-
offspring. The early females reduce this benefit to the last fore, it is no sacrifice at all for those twenty thousand cells
layer in two ways: (I) They lay more eggs, including one to die helping the others, because the ones that die are the
late in their cycle, frequently at the same time the last female others.
begins to lay, and (2) they also lay more slowly, spreading The point can be reasoned out even more rigorously. How
their eggs out over longer periods. Vehrencamp believes that can an altruistic trait spread through a population? Why
ani society is structured by an age-dependent, female-oriented doesn't self-sacrifice work against itself in evolutionary com-
status hierarchy in which the oldest females get both the petition? One answer is to imagine that there are two copies
largest males-the ani is monogamous, like many birds- of the altruistic genes in the population, and that the indi-
and the most fledgling slots. The males' incubation effort is vidual with one copy devotes his altruism to the individual
a function of the social position of their female; the higher with the other. When such a partnership makes sense, "unself-
she is the harder ttey work-and the less work she does, at ishness" will then defeat "selfishness" in the Darwinian race.
least as defined by rates of brooding and feeding the young. A mother has, comparatively, an aging body that is going to
Feeding a flock of pigeons gives a glimpse of the same die soon anyway; it is far better for her genes to help their
phenomenon: a high level of squabbling competitiveness copies in the fresher, younger body of her offspring than to
within a framework of cooperation on other issues (one issue try to help themselves to eke out a few more weeks or months.
on which flock members cooperate is a common flight path). When the slime-mold habitat collapses, all the amoebas will
The other test of nonindividuality that has been mentioned die if they stay where they are. If only a fraction can escape,
here is altruism, the sacrifice of one's own interests to support and forming a partnership allows more cells to escape than
those of another. As anyone who has pondered the question otherwise could, then genes predisposed to the altruistic be-
of genuine unselfishness knows, it is sometimes hard to tell havior will outcompete more individualistic ones. All that is
the ethical difference between sacrificing for oneself (selfish- necessary for this dynamic to work is that the donor and the
ness), and sacrificing for others with whom one has everything beneficiary of the aid have much in common genetically. \
in common. Is that genuine altruism, or is it just another Sexual reproduction, because it mixes the genes of two
form of selfishness? Biologists have not really resolved this parents, decreases the prospects of that mutuality. All other
problem in their own sphere either. Take as an example the things being equal, it inhibits the development of self-sacrifice
relation between mother and child. Mothers generally are will- and promotes the evolution of self-assertiveness and com-
ing to sacrifice a great deal of their time and energy for their petitiveness. Imagine a gene appearing in an asexual organism
offspring. No one calls this altruism, since it is sacrifice in that promotes a willingness to share (or a less intense grabbi-
the cause of reproduction. The mother is working to perpetu- ness). When that asexual organism clones itself, all its off-
ate herself in the next generation; her interests, and her spring will carry that mutation, and there will be a certain
progeny's, are very close to being identical. chance that one individual holding the gene coding for that
On the other hand the word altruism is used in describing behavior will encounter and therefore help a sibling that also
the sacrifice of the slime-mold cells that transformed them- has a copy of that gene. But since a sexual organism has had
evolution of the sisterhood has excluded them. They are made
to m~ its genes with those of a stranger to make offspring, in small numbers, cannibalized in times of protein sh?rtage,
:md smce the gen:s of each parent are equally represented and driven from the nest by force when the sisters deCIde the
In the next generatIOn, the chances of an altruistic gene being time has arrived for their mating flight. (Apparently the
able to help itself in a meeting with a sibling are cut in half. males' restricted role has left them so stupid that they don't
The point can be restated by looking at aggressive behavior. even know the best time to look for females.) An early en-
"S.elfish" behavior t.hat arises in an asexual family has a cer- tomologist, Forel, remarked with some vehemence" . . . The
!am chance of hurtIng itself and hindering its spread because males (of ants) are incredibly stupid . . . the orga.ns of
It hurts other members of the family that carry the same thought are very large in the workers, much smaller In. the
gene .. But under. the. s~me circumstances, the chance of ag- queen, and almost wholly atrophied in the males." Tnvers
gressIveness gettIng In ItS own way is halved in a system of and Hare measured the amount of food fed by female workers
sexual reproduction. The conclusion is that the evolution to their reproductive sisters (the insects that are going to fly
of ?ltruistic behavior is half as likely, and the evolution of off, mate, and try to found new colonies) compared to that
~oclally aggressive, individualistic, behavior twice as likely,
given their reproductive brothers. Their finding w~s that the
In sexually reproducing creatures. females fed their sisters three times more than theIr brothers.
Obviously all this can be taken too far; altruism does exist Since females are three times more closely related to each
among sexual animals. But many biologists believe that such other than they are to their brothers, their result shows that
exceptions only will be found among very close relatives- altruism (in the social insects) exactly parallels degrees of
parents and their offspring, brothers and sisters, and much
less commonly, among uncles and aunts and nieces and kinship.-
Kinship theory has also been used to explain a phenome-
nephews-and that even in very closely related creatures non called the helpers at the nest. These are animals, found
some degree of competitiveness is likely to be found. This in a wide variety of species, that seem to devote their. energi.es
whole theory is called the theory of kin selection, and it has to helping others of their species breed. An ormthologlst
proved very useful in explaining patterns of animal behavior named Woolfenden marked the helpers found in the Florida
Robert Trivers and Hope Hare of Harvard have used ki~
selection to explain the marginal position of males in social • Each sister has two sets of genes. one from her mo~her a~d ODe from her
insect societies. For centuries it has been known that all the father. As explained earlier, it is likely that all ~e slSters 10 the nest have
inherited exactly the same set of genes from the1l' father, so . SO perce,nt of
business of these colonies is kept tightly in the hands of the genes of every sister is likely to be given over to a smgl~ •. Uniform
females . They care for the eggs and nourish the developing copy of the paternal inberitaRCe. Since mothers develop fr:o m fer~lhzed eggs, ,~
young, construct the nest, keep it clean and well ventilated unlike males, they have two gene sets themselves, and In malon~ the sex ..., ~l . . ~r
cells1O'15e deposited in their eggs they draw alternate fr~m either on~. .
guard it against enemies, and repair it when the nest is dam~ If there is a unique gene in one set th. not appear 10 the other, It .x\.. \
aged. They scout for food, fight for it if need be when it is will be handed down to every other offspring. . ' " #-
The result is that there is a SO percent chance that an~ two sisters wIll V
found, ~nd ?ring ~t back to the nest. They mark off, defend, have identical copies of some gene hand~d d~wn by .thelr mother and a y.rJ'"
and mamtam theIr nests' territories. If they are ants that 100 percent chance that they will have ldenhcal copIes of t?-0se b~nded v..
down by their father. Adding these up, we see that any two sisters Will be ,.,." V'
garde~, it is the females that tend the crops; the female army
:mts pillage and sack everything in the path of their maraud-
related by ~ + Ii> = 'l4 (or 100 +SO = 150).
By contrast a sister will share with her brother none of the genes 10- ~
. f'-
oJ"
,-
Ing columns; female d~mesticators tend their aphid herds. herited from her father, and only half those inherited from their mother. . ti''''
Males never take part In these activities; something in the Their degree of relatedness is 0 + \4 = \4 (or 0 +
SO = SO). t,.; \.-
('-':'vj. .~\ ~ 'A •
.. _ )~ ~/J~I""" .
64 / WHY MALES EXIST The Consequences 0/ Being Sexual / 65
scrub ja!.. He fo~nd that out of seventy-four cases, helpers also rewarded for their altruism through the breeding of more
were assisting their own parents forty-eight times, a father and kin, but more important is that the helpers have improved
a stepmother sixteen times, a mother and a stepfather twice a their prospects of being able to raise their own family. One
brother an.d his mate seven times, and an unrelated pair O~ly reason these ideas are advanced is that the helpers do not
once. Having the benefit of a helper's time and attention in- work very hard; the birds themselves do not act as though the
creased the survival rate of chicks hatched in the nest by major reason for their being is to make more kin. What they
nearl~ th.ree-fold. The helpers did not lay eggs; their main seem to be doing is performing just enough work to com-
co~tnbutlOn seemed to be in detecting and mobbing preda- pensate their parents for the nuisance of being underfoot and
tonal tree snakes. A kin selectionist interpretation of this be- competing for food all the time, so that their parents won't
havior is that it is adaptive because the tree snakes make drive them off. The parents, of course, have an interest in one
establishing a nest without a "guard" a chancy business. A of their own progeny's inheriting the property, so they will let
young bi~d will reproduce better by staying with its parents the young birds get away with less work. Thus there are at
and helping them make more of its brothers and sisters than present (at least) two explanations as to why young jays help
by trying to initiate a nest on its own. If the tree snakes were out at relatives' nests: First, because whatever effort they do
to be wiped out, then the balance of benefits would reverse expend gets used in making kin, and second, since relatives
and the quality of familial devotion in the scrub jay would have a reason to be more tolerant of them, the helpers will
suffe~. Kin selection nas also been invoked to explain the be able to get what they want (residency) with less work.
prac.tt~e, among ground squirrels (Spermophilus beldingi) , If they tried to help at the nest of an unrelated jay, the young
of glVlng an alarm call when a predator appears. Paul Sher- birds would have to strike up a true symbiotic relationship,
man, of the University of California at Berkeley, was part a business deal, in which they gave as much value as they
of a team watching a colony of these squirrels respond to received. Why should they bother with what might be real
predators (weasels, badgers, dogs, coyotes, and pine mar- work when they can get by with just loafing around at home?·'
tens). He found, first, that voicing an alarm call was danger- Animal societies are not always such a picture of striv-
ous; the alarm givers were stalked or chased by all five groups ing, pushy, self-promoting individuals; occasionally one runs
of pre~ators more often than noncallers. But a squirrel was across observations that seem to be virtually Christian par-
more likely to incur this risk if it had kin in the area. ables. One of these was contributed by Anne Rasa of the
.Kin sele?ti?n i~ immediatel! plausible to a lay human Max Planck Institute in West Germany. She was doing a
b~mg, but It IS sull controversial among professional biolo- long-term study on mongoose society when one of her males
?IStS, many of. whom doubt that even the prospect of benefit- (Male 5) contracted kidney disease, weakened rapidly over
Ing close relattves would necessarily cause an animal to select a month, and then died. Mongooses are monogamous mam-
charitable and generous behavior. For instance, some orni- ' mals (one of the very few), and live in groups of pairs orga-
thol~gists doubt that scrub-jay helpers get enough repro- nized in a dominance hierarchy. Male 5 was fairly low-rank-
ducttve success from being "aunts" and "uncles" to make ing, but, as his illness progressed, the band allowed him
t~eir behavior adaptive. These biologists believe that the young priority access to food. Further, while before his illness he
birds ~tay at their relatives' nests because good spots to make was only rarely in physical contact with the top couple, when
scr~b-Ja~ nests ~re ,very limited, and the helpers hope to in- he became sick the top-ranking pair increased their periods
hent their relattves territory. Of course the young birds are of contact with him tenfold, and, toward the end, spent the
whole of their resting periods in contact with him, grooming
him more and more, and licking him as his efforts to stay
clean failed. Ms. Rasa believes that her mongooses were so
solicitous toward the failing male because a larger band can CHAPTER
vn
mount a more vigilant defense against birds of prey, the
mongooses' major enemy in the wild.
To some this view of natural relationships may paint a de-
pressing amount of self-centeredness. I would be the first to
admit that there are other ways of talking about natural so-
cieties; over the centuries there has been a regular alternation THE EVOLUTION
of descriptions that stress social cooperativeness in nature and
those that emphasize individualistic self-advancement, and no OF GENDER
doubt these zigs and zags of fashion will continue for cen-
turies yet. But for the purpose at hand, for investigating the
behavior associated with the evolution of sexuality, this em-
phasis seems like the right one. Compared to sexual creatures, THE ARGUMENT SO FAR RUNS AS FOLLOWS: SEX--GENE-MIX-
) asexual or less-sexual organisms have achieved higher degrees ing~volves when the members of a species find that their
of social discipline, more elaborate organizations of mutually lives' outcome depends on how well they respond to sogilU
dependent specialists, and more striking examples of self- competition. These contests are usually not directl~ competi-
sacrifice and altruism. Sexual creatures have developed more tive. in the push-versus-shove sense; the affected anImals may
elaborate ways of leading an independent and self-sufficient never see each other. Rather they are competitions of skill,
life while competing with other animals with similar needs. competence, and efficiency. The animals that reach th~ im-
There is an ironical aspect to this: Sex requires mating, which portant resource first do so not because they fought for It, or
is a very intimate activity. In other words the very adaptation out of good luck, but because they were more of a master of
that animals have turned to to help them compete with other the conditions at hand than other members of their species.
members of their species requires them to cooperate with The more important this sort of indirect competition be-
their competitors, at least briefly. While sexual reproduction comes the more likely it is that specialists will evolve. Animals
seems to promote independence, it certainly also makes sexual will appear that are better equipped to deal with ~ome of the
creatures dependent on one another for gene transfer. The situations they might encounter, and less well SUIted to deal
question of how these issues of cooperation and dependency with others, than a generalist would be. When this happens
are resolved in a context of strongly independent individuals sexual reproduction becomes adaptive, since it allows parents
is an important one, and it is with this question that the rest to have, as it were, a "complete line" of progeny; some
of this book is concerned. offspring out of the "line," ideally, will tum out to have the
equipment required for whatever specialization has the most
openings, the best opportunities, for the time and place at
which the progeny become self-supporting.
However, evolution is not just a matter of animals respond-
68 / WHY MALES EXIST The Evolution of Gender / 69
ing only to their outside environment. Tools can remake their surances might need to be made as whether the prospective
users, and often do. Sex may have been selected as a way of mates are appropriate for each other, whether, on the most
allowing parents to compete more effectively with other par- basic level, they are in fact adults of the right gender and
ents, but sex itself influences the nature of the creatures that species. Someone is going to have to get that ~formation
use it. It makes them more self-sufficient and independent, and together and transmit it clearly, quickly, and credibly to the
enhances those qualities we refer to when we speak of animals' other mate. There may be a surplus of mates and some point
\ being "wild and free." in choosing among them. If so, then there might be an issue as
So sex is selected in the first place when the social context to whether the mate in demand is going to have to evaluate
in which animals live becomes more competitive, and to the the several candidates and choose one or whether the surplus
extent that it has any independent influence on the nature of mates will have this burden imposed on them as well, in which
those who use it, it makes them even more competitive and case they will have to select a champion by themselves and
independent. Yet at the same time, as paradoxical as it seems, then send the winner on. Finally there is a question as to how
it is impossible to have sex, gene-mixing, without an act- the labor of getting into the reproductive state is going to be
mating-that often requires a profound degree of intimacy, divided. For many animals the transition from foraging to
cooperation, and mutual vulnerability. Many issues need to be breeding is a drastic one, involving many changes in behavior
resolved before two wild animals can mate-where, when, and physiology. It would be convenient to avoid putting these
who, and how, among others-and for each one of these issues changes off as long as possible, that is, until the prospect of
the same question arises: Who is going to bear the burden of being mated was both imminent and certain. The ideal for any
the resolution? Who is going to be inconvenienced most? Every one animal would be to get so much attention from its mate
animal would prefer to mate at a place and time that best that it could synchronize the transition into the reproductive
preserved the order of its daily routine. (The very fact that state by those efforts alone.
these creatures are sexual at all suggests that they are special- If all these issues were resolved in favor of the same animal,
ists at what they do, and therefore especially likely to suffer then when it was most convenient for that party, a partner
from diversions.) Some animals live in multisexual colonies or would appear exactly where that mate happened to be; the
as mated pairs, and for these where and when may not be a partner would communicate whatever information was of in-
problem. (There are a number of species of anchored marine terest, and would set up a beat or rhythm of some sort that
invertebrates, for instance, in which the sexes live intermixed. would allow a fast, synchronize-crtransttion into reproductivity.
Fertilization is accomplished through a simultaneous, massive If more than one such mate appeared, then the candidates
volley of sex cells, in which both eggs and sperm are dis- would settle among themselves the question as to which one
charged into the water. The discharge is triggered by a specific best fits the mating requirements of the favored mate, and send
environmental signal, such as the angle of light penetrating the on only that individual.
water, to which both genders react in the same way at the same The remaining pages of this book argue that this is fairly
moment.) But most animals live sufficiently dispersed so that close, more often than not, to the deal that females actually
some searching is done by one or both mates prior to mating. do get in nature. When a female moth wishes to mate she re-
In all such cases there is a question as to who is going to bear leases a tiny quantity of pheromone and all the downwind
the burden of the search. males within hundreds of yards begin flying toward her.
The mating interaction imposes other burdens as well. As- Female salmon choose, for some reason, to mate in a place
that is enormously inconvenient for a fish that lives in the sea; It may be that males exist, as males, only in order to cater
but whatever other problems this habit might make for her, to female preferences. In the first chapter the question was
acquiring a mate is not one of them. Whatever stresses and raised as to how creatures as apparently wasteful of their
strains are involved, male salmon will follow her wherever she energies as males could ever have evolved. After all, there are
goes. The males of a number of species of mammals, including other sexual reproductive systems in which all the members of
giraffes, routinely taste their females' urine in order to moni- the species are clearly involved with the manufacture of off-
tor her estrus cycle and be able to mate with her when she is spring, the simplest of which is bisexuality, in which everyone
ready-a behavior which guarantees these females a very effi- makes both sperm and eggs. How could a system in which half
cient, convenient fertilization. the species abstains from making this sort of direct contribu-
The reason males behave this way was mentioned in the first tion ever establish itself against the competition of these alter-
chapter: they have a problem with competition. What a female natives?
does to reproduce: build up eggs and superintend their de- One answer might be that females who retain control over
velopment, takes time; what a male does-find fertile females the circumstances of their matings can use that control to be-
and fertilize them--can take next to no time at all (depending come much more productive and efficient. In these cases
on the social situation) . This means that males will usually females that hired an assistant who did nothing but minister
find themselves reentering the breeding pool much faster than to their reproductive convenience might outcompete bisexuals
females, and that a population of competing males will arise. who tried both to accumulate protein for the eggs and to give
In such cases females will have a choice of suitors; naturally and get fertilizations. There are a number of ways in which
they will use this leverage to pick the male that makes matters having males as go-fers of the mating interaction might make
most convenient for them-the male who is where they want, females more effective. One is that females are, as stated, spe-
when they want, and who behaves properly in other ways as cialists, and a system of competitive males would allow them
well. The fireflies that one sees flitting and flashing about in to continue to pursue their specialization, whatever it might
the evening are usually males; the females are carefully se- be, as long as possible. A second possibility, which by no
questered away in the underbrush, sheltered (one assumes) means excludes the first, is that competing males give females
from nocturnal predators like bats. Meanwhile the male has to a very useful degree of control over their own reproductive
fly around advertising himself in a most conspicuous manner. schedules. There are two schedules involved: the development
When a female catches sight of a flash pattern that promises a of the fertilized egg, to the point of release, and the packaging
male of her own species, then, and ouly then, does she respond of progeny sets over the female's entire life-span, so that she
with an answering flash (often weaker than the male's). As . can have a large number of litters, or clutches, or whatever.
mentioned earlier, there are firefly predators that mimic these An asexual female has total control over both these sched-
flashes and capture and eat the males that land in response. ules and can adjust them to take maximum advantage of
If it were the females that were flying around looking for whatever possibilities there are in the environment and her
males, then they would be the ones to run all these risks. But physiology. But a sexual organism has become dependent on
males have to run them, because they have competitors; if they an external factor: the arrival of other genes. A delay in their
play a cautious, careful waiting game, then all the females in arrival, or a general lack of predictability on when they might
the area will be fertilized by males who are willing to run the arrive, could prevent a female from keeping either of these
risks of mating with the females on the females' own terms. schedules from running at their optimal rates. It is a mistake
72 I WHY MALES EXIST The Evolution of Gender I 73
to think that the egg sleeps away in the female like a princess and respond with a small sperm ejaculation. The. fema~es in-
in a fairy tale, waiting only to be awakened by the kiss of the ect this ejaculation to see if it belongs to the nght kmd of
sperm. By the time the sperm first appear, each egg has had a ~ale; if it does, they release their eggs. This ~ct ~timulates
long history; it has been constructing the biochemical equiva- the males to a massive sperm ejaculation. The p~mt IS that the
lents of machine tools and assembly lines, stockpiling subas- whole process was initiated by the females, even If the first step
semblies, preparing energy sources, and generally tooling up they took was a subtle one; it was the females that defined the
and gearing up for the long developmental process ahead. It is moment when the mating interaction took place. _L
true when the sperm arrives that the cellular divisions and dif- An especially persuasive dramatization of the idea that fe- )f-
ferentiations begin; but none of this activity has anything to male convenience has shaped the evolution of the male gender
do with the genetic material brought by the sperm-that is not is found in the anglerfish. These are a group of deep-sea dwell-
unpackaged for hours. Dividing and differentiating is some- ers, about one hundred species strong, who get their name from
thing that the egg does by itself, at least in the beginning, in the foraging practises of some of the females, who dangle a
response to a sperm merely having arrived. There are a hand- little phosphorescent lure in front of their mouths to ~tt~act
ful of species (nematodes, planarians, earthworms, minnows, prey. In many species of this group the males los~ their !aw
goldfish, and salamanders) in which the sperm does nothing teeth early in their youth and thereafter draw thm no~r~sh
more than this; its genes are never expressed in the offspring ment entirely from internal food stores. They replace .thelr Jaw
at all. In other species the influence of all the prefertilization teeth with a set of pincers (whose purpose has nothmg to do
activity extends throughout the whole life of the offspring. A with food) and set off to search for females; if they do not find
good example is that of a snail whose shell can spiral either a female before their food stores are exhausted, they will die.
clockwise or counterclockwise; which direction the shell of any The males have enormous nostrils-as much as one-quarter of
specific snail will curl is already a settled issue by the time the their head-and extremely well-developed eyes for an animal
sperm arrives. Biologists can induce the eggs of a number of living at depths where no sunlight ever penetrates. They h~ve
I species, including frogs and mice, to develop into perfectly

healthy adults without any fertilization at all. In short, the
relationship of an egg to a sperm is not that of a seed waiting
been called "sexual guided missiles," but are really more like
sperm with sensory and transport systems. If and when they
find a female they lock their pincers onto whatever part of h7r
quietly for its sun and water, but that of a busy industrial body they bump up against. The circulatory systems and skm
executive with a packed schedule, for whom the arrival of the surfaces of both sexes merge. The male loses his eyes and fins.
sperm is just one event, even if an important one, among many. The two become, literally, of one flesh.
For such an executive punctuality is important, and a com- At this point, collected specimens seem to show, the f~male,
peting-male system forces the males to be punctual, since only who is already substantially larger than the male, begl~s to
the punctual males get to reproduce. accelerate her growth, becoming, sometimes, a hundred times
There are many natural systems that fit into this female- his size. The male also grows a little, drawing nourishment
service idea of male purpose. One is a marine worm (Grubea from the female, and enters into sexual maturity. The female
clavala) that reproduces via the following minuet. First the develops her eggs. The male-female merger allows the male to
females build their eggs up to a state of readiness. Then they monitor the female so that when she ejects her egg case into
advertise that readiness by ejecting a little squirt of egg protein the water the male's sperm follow immediately. The egg ca~e,
into the water. This squirt alerts the males, who come closer which is the size and texture of a kitchen sponge and con tams
hundreds of thousands of eggs, begins to swell and suck in routines disrupted by the need. to hun~ up a ~a~~ herself.
water, and with the water, sperm. It floats to the surface where Every species, and group of species, has Its pecuilarltles, how-
the fertilized eggs hatch and feed. Eventually the weight of the ever and the anglers are not representative of the usual case.
developing young draws them back down to their parents' As ~ rule males conform to female convenience because their
world. speedier mode of reproduction builds up a population of com-
Ichthyologists call these males parasitic males, and no doubt peting males that gives ~em~les a c~oice ~f mates. When so~e
when a female is first seen with one (or sometimes more) issue involving the matmg mteractlOn anses, the females Will
sticking out of her the resemblance to a parasitic lamprey pick the best and/ or most convenient candidate. Thus those
dangling from a lake trout is striking. But the resemblance is males that conform to female preferences will have greater
only a casual one. The eels get no help from their trout hosts. reproductive success than those that don't. The anglerfish. are
The angler females advertise for males, both by releasing monogamous, though, in the most extreme sense pOSSible.
pheromones and, judging from the size of the male's eyes, by There is probably no population of competing males driving
some kind of visual signal of which we know nothing. Then the system here. In fact males are rare enough so that an
they accept the male into their own tissues. Any immunologist angler female does not, apparently, even commence her final
who has been struggling to make it possible for humans to ex- growth surge until she already has a male in her poc~et. She
change simple skin grafts will appreciate what must go into an waits for the arrival of the males rather than tunmg her
ability to combine separate, unrelated individuals. (Another growth rate solely by the possibilities of the environment, and
bit of physiological acrobatics tossed off by the angler is that when one does finally appear, she supports him. It is very
even though the circulatory systems are linked, the sex hor- rare for females to go to that kind of trouble for a male.
mones of the female do not affect the male testes-nor the When one looks at the problem from another angle-the
male hormones the female ovaries-adversely.) distribution of bisexual versus gendered species-the theory
The angler lives in a habitat with no landmarks-not even that males evolved for the convenience of females seems to
a horizon. Food is not plentiful; the population density is low; pick up some support. In general bisexual species are found
females are widely dispersed. It is difficult to find anything in among snails, sponges, slugs, and worms, creatures that ac-
any given period. In these conditions the female anglers have quire their food by filter-feeding, continuously processing a
solved the problem of being mated at the right times by evolv- relatively low-quality intake. Bisexuality is not found in spe-
ing a system in which each female has her own little toy, cies that look for isolated little bits of high-quality food,
pocket-sized male, which she keeps with her and supports, and species for whom the issue of getting there first is important.
who in return has sex with her when and where she specifies. Bisexuality is also found in environments that support low-
The angler male frees the female from the need of roaming population densities: in the higher latitudes, the deeper zones
around the ocean searching for males and allows her to pursue of the ocean, and the fringes of the richer habitats. This phe- ,I."
her notably low-energy form of foraging, in which she waits nomenon is well-enough documented to have its own name- '1'
patiently for her prey to come to her, without sexual distrac- spanadry, the decline in the proportion of males toward the
tions. borders of a species' range. American eel males are more
The anglerfish illustrate how important it can be for a likely to be found in southern waters than in northern. M~le
female to have a male on her terms, and not to have her own producing species of copepoda (copepoda are the marme
The Evolution of Gender / 77
insects, tiny, enormously various and abundant, herbivorous twO subspecializations: a manufacturing and a .se~ic~ aspect.
invertebrates) fall off regularly as greater depths of water are F males are what we call the animals that speCialize m ~an~
sampled. In one surveyed millipede (Polyxenus lagurus), the f:cturing; males, those that specialize in service. Puttmg .It
.-, fraction of males fell from 40 percent in France to zero per- still another way, males have been devised by females to aid
cent in Finland, with a steadily faIling gradient in between. them in their competition with other females.
If males evolved to give females a finer degree of control
over their mating circumstances, then one would expect to
see bisexuality where and when this degree of precision was
( less important. In general, a survey of bisexual species does
seem to point in that direction. When the production of males
falls off, it seems to be where females are less often affected
by each other, either because population densities are low, or
because their system of foraging is inherently noncompetitive.
A common explanation for bisexuality is that it evolves
where it is important not to miss any mating opportunities.
On the odds, only half the encounters between two gendered
individuals will be between potential mates; any two bisexuals
can mate.' Since bisexuals tend to live in sparsely populated
habitats or are slow-moving, it is more important for them
to convert every encounter into a mating. Darwin himself
devised this theory in a famous work on barnacles. This is
a plausible answer to the question: why bisexuality instead
of sexuality? But it is possible to turn the question around
and ask it differently: why sexuality instead of bisexuality?
No doubt it is useful to bisexuals that every meeting be a
possible mating, but why shouldn't all creatures be endowed
with that flexibility? Why narrow the range of candidates
at alI? No doubt it is an advantage to (some) bisexuals to be
able, in extremis, to fertilize themselves and start a new col-
ony single-handed. But shouldn't we all be able to do this?
Having a system of males closes down these options; what
are the compensating advantages? One answer to this ques-
tion is that when animals find themselves living in a highly
competitive environment the reproductive cycle splits into
• As Woody Allen has pointed out, bisexuality doubles the chance of get-
ting a date on Saturday night.
The Prisoner of Gender / 79
that have just this ability of assessing the social situation and
choosing their gender accordingly. In one experiment, when
the young of a certain marine snail (Crepiduia) were isolated
CHAPTER in an aquarium, 30 percent in one sample and 10 percent of
a second began making sperm. When they were put in an
VIII aquarium with females of their species, 90 percent of both

samples became males. The longer the association with fe-
males was maintained, the more time the snails spent as males.
The experimenter concluded that the important physiological
THE PRISONER stimulus was the tactile sensation received by each young
snail on his penis. When his penis stopped being stimulated,
OF GENDER- then, and only then, did he switch over and become a fe-
AN UNRESOLVED MYSTERY male."" The advantages of this flexibility in strict Darwinian
terms, let alone its common-sense appeal, are so obvious that "''-,'\ ,,\
I cannot imagine why the vertebrates, by and large, have lost ~,h
this ability. 1 !'(I' ".
SO FAR ALL THE IMPORTANT QUESTIONS HAVE HAD ANSWERS, Whatever the reason is, gender rigidity is not a necess~ ~,,,
albeit, in most cases, speculative ones. But there is one fea- part of being a vertebrate, because there are a few that retam I'·
ture of gender which seems inexplicable to me, and for which this power. One is the bluehead wrasse, a fish that lives on .A
no satisfactory explanation seems to exist in the literature. Caribbean reefs. The species is divided into two size classes:
~ [ This is the fact that most vertebrates seem to allow their small fish, of both sexes, with variable coloration; and larger
-' parents to determine their gender, at conception, rather than fish, all of which are male. These latter are very distinctly
~<"'" making that decision themselves later on in life. By contrast colored, with a blue head, green body, and two prominent
')
-<: there are a great many invertebrates that can switch from one black bars separating the two colors. The large males set up
gender to the other, depending on where the advantages are. territories near the "leeward" side of the reefs, where, when
Gender flexibility has many benefits. For example, making eggs are released, the currents carry them away from predators
sperm takes less energy than making eggs, so when several that live on the reef. Spawning occurs daily, throughout the
species of worms are starved they become male; when fed, year, around midday. "At this time," a report on this species
they switch back to being female. (There are two genera of says, "most of the sexually active fish gather at a specific site
orchids-Cycnoches and Catasetum-in which flowers that on the reef. There the larger bluehead males set up temporary
grow in the shade become male while those that grow in the spawning territories along the outer rim of the reef while the
sun become female.) 80b When there is an ecological advantage smaller . . . males gather just inshore, . . . often massing
to being one sex or the other, these creatures can follow that in the hundreds." 100 The females, which can spawn every
advantage. Sometimes the benefits of gender-switching might day, attempt to mate with the larger males, sometimes even
spring from the social circumstances, such as when there are waiting in line if a large male is occupied with other females.
many females in the area it is better to be a male. There are Fertilization is external, and stimulated by a "spawning rush"
a great many invertebrates-sponges, parasites, mollusks- in which the male and female release their sex cells simul-
80 I WHY MALES EXIST The Prisoner of Gender I 81
taneously at the apex of a rush toward the surface. While the female, who tries to change sex and become a male herself.
smaller males do get some mating opportunities, the large If the group is one of those with two dominant females, they
males mate far more frequently, often fertili zing as many as might each change into males and then divide the territory
forty times a day, and sometimes, one hundred. Thus being and the "harem" of other females between themselves.
a large male is a much more attractive line of work than
For approximately half an hour after the death of the male
being either a small male or a small female, and, when blue-
the dominant female continues to behave . . . as a normal fe-
head wrasse females get large, some of them do indeed switch male. . . . Approximately one and a half to two hours after
sexes and try to establish a territory of their own. When a male death, maleness appears in the form of the special male
dominant dies, or is removed by a curious ichthyologist, all aggressive display that the new "male" starts performing to the
the large members of either sex compete on a more or less females of its group. The assumption of the male aggressive role
equal basis to replace him. can be virtually completed within several hours, when the
A related species, the cleaner wrasse (Labroides dimidi- "male" starts visiting its females and territory borders. The
a/us), makes its living by cleaning parasites from the jaws switchover to male courtship and spawning behavior . . . can
and gills of a wide range of other fish that visit permanent be partly accomplished within one day and completed within
cleaning stations maintained by the wrasse. (Fish swim from two to four days.
out of sight right to a specific area where they stop and wait.) The virtues of gender-switching are not confined only to
The social unit consists of a single male, a group of three giving females a crack at being male. There are at least two
to six mature females, all of whom he fertilizes, and several species of coral fish (Amphiprion bicinc/us and A. alkal-
immature wrasses of no developed gender, all living at a /opisos) in which males seem to contend among each other
single station, or territory. The largest, oldest individual is for the advantage of being female. These fish, also called
the male; he gets to clean whom he wants. The largest female clown fish because of their variegated coloration, live symbi-
lives in the center of the territory with the other females scat- otically with sea anemones. The clown fish are immune to the
tered around her in various subservient positions. If there anemone sting, and when predators threaten they retreat be-
are two equally large "top" females, then the territory might hind a shield of tentacles; at least in some species, the clown
be divided between them. The male defends his territory fish are known to share food with the anemones. The fish are
against neighboring males and frequently visits the cleaning large enough so that, as a rule, only two adults, a male and
sites of the females, who are comparatively more sedentary. a female, can live on each host. The two fish seldom change
There he feeds and interacts aggressively with them. "The partners, perhaps from the risks involved in swimming to
male is more aggressive," writes D. R. Robertson, a student another anemone. The typical social unit consists of a large
of these wrasses, "toward those females most likely to change female, a single smaller male, and a varying number of even
sex and threaten his position-that is, larger females, espe- smaller subadults and stunted juveniles, none of whom are
cially the dominant one." Robertson notes that there is a spe- offspring of the adult pair. The female dominates the male
cial aggressive display, not seen in either female-female or and they both dominate the smaller fish.
male-male interactions that is employed specifically by males Specifically, the female regularly attack~ the tw~ top-rank-
against the larger females. ing males; the ranking male focuses hIS energIes on the
When the male dies there is a general rush to take over his second- and third-ranking subadults, and so on. Each fish
territory between neighboring males and the largest resident attacks most vigorously the one immediately below him or
82 / WHY MALES EXIST The Prisoner of Gender / 83
her in the hierarchy. This "intragroup social pressure," write female, then fewer eggs and less procreativity for itself would
Hans and Simone Fricke, who studied these fish for three result. The second fish stays a male for the same reason. He
years in the Red Sea, "determines the gonadal development has no reason to be a female; he is already a parent of all the
of the subdominants. Their testes are smaller and show little eggs produced by the pair. Switching gender is not going to
or no testicular tissue. Low-ranking males are psychophysio- change that, and since he is smaller to begin with, he will lose
logically castrated." progeny, not gain any. It is true the female harasses him, but
When the females were removed from twenty-four c1own- that might be to remind him to stay out of her place, not to
fish pairs, eighteen of the males turned into females and re- keep his gender. And the little fish stay sexless and small
cruited new male mates (of unknown origin). Some began because, if they tried to be male, the resident male would
laying eggs in less than a month. When different-sized males harass them to death by driving them away. (Conceivably
were paired experimentally, it was always the largest and they might try to be very small females.)
more dominant that changed into a female. Interestingly, the The point is that in many species creatures have the capac-
females refused to change back again; pairing of females ity to follow opportunity from whichever gender it beckons.
resulted in the death or serious injury of one of them, not in The advantage of being able to fine-tune one's sexuality to the
a switch to masculinity and subordination. conditions immediately at hand seems obvious. It is very com-
The Frickes explain this system by arguing that everyone mon in sexual species for a significant fraction of the males )
is competing to be a female. The dominant female prevents to be shut completely out of all mating opportunities. Why
the production of more females by actively suppressing those don't those males then try to become females, no matter how
males that are the most likely candidates for gender-switch- incompetent and inexperienced? And yet there are very few
ing, while those males suppress other males that threaten to gender-switching vertebrates and no warm-blooded animals
get ahead of them in the queue to be an egg layer. The Frickes at all with the knack. Gender in all these species is determined
do not say what the advantage is in being a female, or why at conception. It apparently is decided permanently by the
the top-ranking female should care one way or the other what parents alone, and by and large, for whatever reason, verte-
gender the second-ranking clown fish chose for itself. One brate progeny seem to have allowed this important decision .\
"
might imagine that the second-ranking male would be over- to be made for them.
joyed if the third-ranking fish were to choose to be a fe-
male; this would give him two females to fertilize. What
would be a real problem for him would be if male three
stopped being "psychophysiologic ally castrated" and started
fertilizing the group female instead of him. Another interpre-
tation might be that all the fish are really competing over the
most secure spot inside the anemone's tentacles. The larger
fish takes the best place; the second larger the second best,
and so on. Each fish then adopts the gender that fits its life
situation best. The largest fish becomes a female because, be-
ing largest, it can make more eggs than anyone else. If it
stayed a male and let one of the smaller fishes become a
Doing the Paperwork and Other Issues / 85
how the partners have to learn where to meet when the
female is receptive. If a choice of mates is to be made, the
chooser has to acquire enough of the right kind of informa-
CHAPTER tion to make a sensible decision. On the simplest level, it is
important that mating interactions involve two creatures of
IX the same species and the right maturity level but of opposite
genders; otherwise they are absolutely certain to be a com-
plete waste of time. Other values can enter into the mating
choice as well. Somehow all this information has to be gath-
DOING THE PAPERWORK ered, translated into transmissible form, then transmitted, re-
ceived, and decoded. This can be a lot of trouble.
AND OTHER ISSUES If one looked at the question of "paperwork" abstracted
from the realities of sexual politics, one would conclude that
females ought to be the ones to shoulder the burden of the
paperwork because the issue is more important to them. A
.
MANY ISSUES HAVE TO BE SETTLED AS MATING UNFOLDS , AND , female places a larger fraction of her reproductive energies
III p~rt because it is such a departure from the ecological, at risk in a single mating than does a male. Fertilizations for
physIOlogical, and social routines of everyday, the resolution a male are (once a female has been found) cheap and fast.
of each one of these issues might demand a considerable A male will seldom find that he has sacrificed an opportunity
amount of inconvenience, stress, and risk. Two such issues are to fertilize one female or females because he took too long,
time and place. Often all the members of both genders live or exhausted himself, fertilizing others. Each new female is
scattered over the landscape; in other cases the females live in therefore all gain; there is much less need to weigh alterna-
groups but the males forage elsewhere (sometimes because tives and make choices. The opposite is true for females.
the females actively repel any male homing in on their terri- Therefore what one might expect is that once two mates came
tory outside of breeding season). together, the female would actively explore the male, subject-
A third issue is who-if a choice is available, which one ing him to a searching physical and mental examination,
should be the mate? A mate might be preferable because he while the male, in his tum, would demand fewer tests of the
(or, for that matter, she) makes the mating emotionally and female.
physically convenient and comfortable; because he or she Half of this prediction is confirmed. Males are, in fact, less
has control of a valuable resource; or because he or she has discriminating than females. In some insect species, males can
an. intrinsic, personal attractiveness. In the terms used here , even be seen courting females of the wrong species. (Some
thiS last means a genetic superiority, an inheritable advantage, male flies have been seen mating with raisins.) Male frogs
and that advantage, in tum, might speak to an enhanced eco- and toads, particularly in those species that breed in aggrega-
logical, or physiological, or social adaptiveness. (Many biol- tions, clasp male and female alike. Male elephant seals mount
ogists believe that an intrinsic genetic superiority is the most females whether they are pregnant, giving birth, postpartal, or
important issue of all in mate choice.) fertile. There are even a number of species of orchids that
These issues require that information be exchanged. Some- pollinate themselves by "parasitizing" the sexual indiscrim-
86 / WHY MALES EXIST Doing the Paperwork and Other Issues / 87
inativity of male wasps. This phenomenon was discovered in one species of water strider (a Rhagadotarsus) courts through
the late nineteenth century when a French botanist living in the propagation of surface vibrations; male Sceloporous liz-
Algeria, A. Pouyanne, noticed that the flowers of one orchid ards do push-up displays; male tortoises nip the female and
species seemed to be visited only by the males of a certain ram their shell against her. There are all the sounds of spring:
wasp species (Scolia ciliata); the females were completely birds, and crickets, and tomcats.
indifferent. When Pouyanne investigated, he was so startled We ought to look at one display in a little detail; perhaps
by what he found that he accumulated observations for twenty that of rabbits will serve. It has many elements. First, there is
years before he published a word. Eventually he and other "courtship chasing," in which the buck pursues the doe back
botanists showed conclusively that in this and other cases, and forth across the field:
the males copulated while in the flower and received no food .
These facts and the rough visual similarity between the flower . . . chases are interspersed with long intervals of false feed-
and the female wasps convinced the investigators that the ing, in the course of which both animals retain their alertness,
orchids imitated both the odor and appearance of the females. and the buck will sometimes edge toward the doe until he is near
The orchids thus enticed the males into a bout of sexual activ- enough to attempt to rush her.
ity that ended by the males' carrying off pollen and therefore
They displayed "amatory behavior," such as licking and
advancing the sexual ambitions of the orchids. "It may be that
nuzzling:
those who would reject the evolutionary approach to an under-
standing of life," wrote a botanist of these flowers in 1937, It is not uncommon for two rabbits to be lying face to face
"and who prefer to regard the world as the product of Special licking each other's muzzle and ears for a half hour or more. In
Creation, will lean a little more lightly on human weakness most cases the doe then stretches out on the ground and the buck
\ when they discover moral turpitude among the insects.'" sits facing her, so that he may reach the back of her head and
Once the female wasps have emerged in large numbers, inci- ears, which appear to be favorite places to be curried.
dentally, the number of "parasitic" copulations declines rap-
idly. Another behavior was "tail flagging":
Males are less discriminating than females; this much is In this commonly seen form of behavior the buck elevates
true. But when one examines a representative range of mating his haunches so that he walks with a stiff-legged gait, and lays
interactions, one does not see the female busily checking over his tail Bat along his back so as to display its white underside.
a male, examining his good points and bad points like a buyer . . . Various accompanying movements are performed, includ-
at a horse auction. Instead, as a rule, the females simply sit ing "false retreat" in which the buck walks stiffly away from the
there, often looking elaborately uninterested, while the male doe for some six yards, giving her a full view of his elevated tail.
engages in a colorful, complex, and raucous communication He will then return to her and repeat the performance, some-
called a courtship display. times three or four times in succession. Another accompanying
movement is the "parade" in which the buck circles the doe at
Quite a number of these displays have already been men-
about two yards' distance, with tail elevated and his rear quar-
tioned: the sumptuous hut of the bowerbird, the complicated ters twisted toward her. . . . The parade is not always circular,
dance of American grasshoppers, the bands of turkey brothers, but is sometimes conducted back and forth along a line in front
pinwheeling in synchrony around the female. The list could be of the doe with the tail twisted at each passage in the appropriate
extended indefinitely. Fiddler crabs wave their claws; at least direction.
The rabbits also practised "epuresis" or "en urination " in and low; wet and dry, and so on). Exactly the same points
which the male (usually) squirts a jet of urine at his par;ner: have been made about the calls and plumage displays of birds.
The buck may merely turn his hind quarters toward the doe In its main habitat the Australian robin (Petroica mullicolor)
and shoot out a jet of urine backward, but some form of circling males are a bright red, white, and black, and the females a
round th.e doe is more often involved, frequently preceded by camouflage brown. In the small island populations, whatever ...,
ta,l flaggmg. A very common method is for the buck to run past was keeping this system disciplined collapses: hen-colored
the doe about a yard from her and to twist his hindquarters. males and cock-colored females are often seen. The theory in
Southern notes that it is remarkable how rarely these running both lizards and birds is that when there is a risk that the
shots fail to find their mark. A less common method is downward wrong sets of genes might get joined, the males carry unam-
enurination, in which the buck leaps over the doe and emits a jet biguous descriptions of their own genes and assert a sexual
of urine as he passes over her.
truth-in-labeling; when the risk ends, so does the need for
The effect on the doe is variable ... but in a few instances
definite stimulation is observed. elaborately error-free descriptions.
This explanation has gained power in particular from .in-
Who is getting what out of all this noise and fuss? The most vestigations into mimetic species, species that look ah~e
widely accepted theory among biologists is that usually the (sometimes called sibling species). (In many cases the dIS-
males are filling in applications, telling the female, at a mini- covery that a habitat was divided among several look-alike
mum, what their species, sex, and maturity level are, and per- species rather than a single one was mad~ only whe? differ-
haps are describing themselves in much more detail than that. ences among the male displays were notlced.) For Instance
One clue is that when related species live close together their _ there was a case found in Haiti of three adjacent mimetic
J courtship displays differ markedly. Some lizards court with lizard species (all of which had been called A. brevirostris).
an extensible chin pouch, called a dewlap, which is repeatedly The males of the northernmost species all had dark dewlaps;
and rapidly flashed in front of a female. On islands where liz- the males of the southernmost species, light dewlaps. But the
ards of the same size compete for similar resources, the males males of the middle species had light dewlaps toward the
?f different species never share the same dewlap color. For northern part of their range and light ones toward the south.
Instance, the three following two-and-a-half-inch long species Their identities were emphasized most strongly where con-
were all found living on the lower parts of trees in Camaguey, fusion was most likely_ This might not prove the "gene-
Cuba: AnoUs homolechis, a dewlap of gray or white, and a labeling" hypothesis, but it surely fits it nicely. In a series of
body color of light tan with horizontal stripes and four dark experiments on two mimetic species of European grasshoppers
chevrons; A. allogus, a dewlap of yellow to apricot with three (Chorthippus brunneus and C. bigu/lulus), it was found that
to four reddish stripes and white margin and a body color of in almost every case grasshoppers did not answer calls except
reddish-brown with yellow reticulations; and A. sagrei, a to the opposite sex of their own species. The only way in
dewlap of bright red, dark red, or brownish-yellow against a which cross-matings could be induced was by having the songs
body color of tan brown. Solitary species living on islands of the right mates playing in the background. (In the wild,
that can support just one or two lizard species generally all the male travels about, calling randomly, until a female an-
have yellow to yellow-orange dewlaps with gray-green body swers. Then he shifts into a display song and approaches her.
colors, even though these island lizards come from several dif- The two mate only after exchanging chirps for a while.) Some-
ferent evolutionary lines and live on all kinds of islands (high times experimental manipulation can expose the system even
90 I WHY MALES EXIST Doing the Paperwork and Other Issues I 91
more clearly. In two ponds, each stocked with two species of populated category. This might sound lik~ a l~t of wo~k, but
sunfish, hybridization occurred only in that pond in which the it does not compare with what the male IS dOing. He IS gen-
male's display fins had been removed. erating the data, and to do so he uses all the channels of
It is possible that females can use these "gene labels" to communication open to him: tactile, auditory, visual, and
achieve quite a degree of fine-tuning in their mate choice. On olfactory. He dances, he buzzes, he generates ~he~omo~es. In
Guadaloupe there is only one AnoUs-type lizard, so there is so doing he is laboriously filling out an apphca.tlOn With all
no risk of two species cross-mating. Nonetheless the markings manner of detailed information about who he IS and where
of these males are anything but dull. The species (A. mar- he comes from. The female then evaluates his application.
mora/us) divides into a series of races . . . What the female does is cerebral and might sound more
impressive, but it is really the male that has to bum the
. . . in one of which males have an apple-green body and a
blue-gray head with brilliant orange marbling, while in another calories.
Why should the males do all this work when it is the fe-
males are plain green in ground color but anteriorly and dorsally
males that stand to lose more from wasted matings? The \
have dark blotches tending to run together and set off by pale
cream borders. In yet another race males are pale gray-green answer, obviously, is that the females can afford to wait. While
with brown heads, and there are still other remarkably different males run out of females before they run out of sex cells, fe-
patterns within this one species. . . .". males almost never run out of eggs before they run out of
potential mates. Her eggs will be fertilized, if not now, th~n
Some herpetologists put cases like this together with the soon enough. If a superior male arrives on the .scene, h: Will
observation that dewlap patterns and ecology seem to be asso- get around to her. The difference in repro?uCIiVe tem~1 and
ciated (a male living in a wetter area might show more the existence of the population of competmg males give fe-
orange) and suggest that these lizard males have been selected males the lUXUry of an extended contemplation of the issues.
to reveal in detail the kinds of environmental conditions to But those males who can persuade females fastest that they
which their genes are best adapted. are the ones the females want, who can settle reservations fast-
Fruit fly (Drosophila) females seem to prefer, for whatever est, quiet misgivings most expeditiously, will suffer leas~ from
reason, "minority" males, the less common male types in a interference by competing males and have the most lime to
population. If five males from Texas are mixed with fifteen devote to scouting up additional mates. (In addition, in many
from California, the Texan males do better; but if the propor- species mating involves some risk to a female, either to pred-
tions reverse, so does the ratio of sexual success. (In the ex- ators by exposing her or reducing her mobility, or to the
periment just cited the females were divided equally between hubb~b of male fighting. A male that can establish his quali-
Texan and Californian strains.) Besides being able to pick fications quickly might find himself being rewarded for that
out the less commOn of two strains, they can pick out the least reason alone.)
common in more than two strains. This means that the females Another issue of the mating interaction is who does the work (
must (I) have a preexisting classification system into which of synchronizing the relation. When males and females ma~e
the various males can be sorted, (2) count how many males they both, though to different degrees, have to abandon therr
there are in the sample that fall into each category, (3) com- accustomed habits and adopt new physiologies, behavior pat-
pare and then rank the categories according to the number of terns, and social relations. Often they must both abandon an
males in each one, and (4) accept a male from the least- antipathy to a physical encounter with a creature of their own
kind. An animal might be selected to manage these difficult the male is doing, with his mounts .and dismounts, is ~uilding
transitions itself, or to help others pass through theirs, or both. the female up to a level of stimulatIOn such that she WIll ent:r
As a rule males are selected to manage their transitions on 'nto a receptive posture, called "lordosis". While in lordOSIS
their own and to help females pass through theirs. Once again ~he female is, in the words of one investigator, "in a vegetative
males find themselves adapted to conform to female require- state". She becomes insensitive to many classes of sensory
ments and conveniences, and the reason is the same: any sin- stimuli to which she would ordinarily pay attention. All her
\ gle mating benefits the male more than it does the female. A
male that brings a female into reproductive readiness gains a
set of progeny he would not otherwise have had; progeny that
locomotive reflexes seem blocked. Her body is arched and
rigid, and the pupils in her eyes dilate to t~eir f~llest ext~nt.
The rationale of the repeated penetrations IS found In the
would probably have been fathered by some other male had mechanics of the females' production of progesterone, the
he not brought the female into receptivity. A female that brings hormone that allows the fertilized egg to implant in the uterus
a male into a sexually active state usually gains nothing but a wall (and performs many other pregnancy-related functions).
mating that she would have gotten anyway just by waiting a Rat females do not produce this hormone continually; what
little longer. switches production on are the repeated male intromissions.
So it is not surprising that endocrinologists have found that Females receiving too few intromissions from a male who
male courtship also has a positive influence on the production nonetheless ejaculates do not transport his sperm from their
of female hormones and general glandular changes. Experi- vagina into their uterus. Males seem to be sensitive to the num-
ments showing these effects have been carried out with canaries ber of intromissions females need; in experimental matings
and other birds, reptiles, bullfrogs, and with many small mam- . between strains of rats that required different numbers of
mals. (It has even been found that a female canary exposed to thrusts to switch on the progesterone, the males tended to con-
a richly varied, diverse, male song builds her nest faster and form to the females' needs rather than their own past practise.
lays more eggs than does a female who has to put up with a A variant of the theory that male courtship helps females
more limited repertoire.) The more male courting behavior shift physiological gears is that male courtship overcomes the
female lizards are exposed to, the faster their ovaries grow. It fight-or-flight reflexes so routinely relied upon by animals in
is the behavior, not just the physical presence of the male, that their everyday life. This explanation has been .explicitly ~d
counts, since castrated males, who do not court, do not stim- vanced in connection with the intricate courtshIp ceremomes
ulate increased levels of hormone production. of the manakins, a group of about fifty-odd species of tropical
There are a number of small mammals (cats, rats, rabbits) fruit- and nectar-eating birds. The males of many of these
in which it is known that the mechanical stimulation of copu- species mount joint displays, involving two or more males in
lation, entirely apart from the actual ejaculation, is necessary what is virtually a circus act.
for the female to ovulate. Copulation in rats, for instance, Mercedes Foster, a zoologist from Berkeley, recently pub-
seems a rather cumbersome affair. The male mounts and dis- lished a report on the behavior of the long-tailed mana~in,
mounts the female over and over; then he intromits, or pene- Chiroxiphia linearis. In this species two, and on rare occasIOns
trates her, several times. Finally, after somewhere between five
and eighteen thrusts, depending on the strain of rat examined,
ejaculation occurs. Often then the male dismounts, waits sev-
three, males form long-term mutual attachments, persisting. at
least some of the time from year to year, over many breedmg
seasons and independent of the chosen display site (if the
\
eral minutes, and then begins the whole procedure again. What display'site is changed the birds move as a pair). The season
Doing the Paperwork and Other Issues / 95
begins by these pairs voicing a synchronous call, which Foster
b displaying together in this coordinated fashion, overwhelm
reproduces as "toledo". Unpaired males do not give this call
Yfemale'S normal feelings of aggression and fear at the pros-
and never attract females, and paired males almost never at-
;ect of a close approach by other manakins more rapidly than
tract females except when producing this call. When a female
arrives the birds . . . single male could, plus they will attract more females as well.
a What is there, one wonders, about a male jumping around
. . . move to a display site consisting of a low display perch that connects with a female's hormone system? Why do th~se
and associated vines and branches. One male, or both alternately, displays work? The feeling I get, in listening to or watch~ng
performs a Solicitation Display which appears to stimulate the the displays of local animals, is that they work by choosmg
other male to proceed to a Jump Display. The Jump Display, sounds and motions that reproduce within the female the same
which cannot be performed by one male alone, has a number of feelings that are induced by good environmental conditions.
variants. The two most common are described here. In the Up- In other words, imagine that females are selected to ~e fer-
Down Variant the males perch perpendicular to the length of tilized in a certain range of temperatures, or when. m the
the display branch facing the female. In a coordinated fashion
presence of a rich-looking territory. Such a fem~le .mlght .be
they alternately jump into the air, one bird hanging at the peak
of the jump momentarily before descending to the perch. As he pictured as, at least on some days or in s?~e tern tones, bemg
lands, the second male jumps, and so forth. As the male jumps, a little uncertain as to whether the condItIons of the moment
he gives a wheezy buzzee call. In the Cartwheel variant the males are quite good enough. At such a point a male that loudly
perch parallel to the length of the display branch facing the declares this to be the best day ever seen, or the most mar-
fem ale located at one end. Again they jump alternately, but now velously lush countryside imaginable, who induces in her the
the front individual jumps backward, landing on the spot previ- mood that those conditions would have created had they clearly
ously occupied by the second male who moves forward to the existed might push her over into a positive decision. Certainly
anterior position. As long as the sequence lasts they make a con- listening to birds court makes me feel happier, more expansive,
tinuous moving circle around each other. confident, and ready for adventure.
After the joint display the top male of the pair (always the
same one) performs a special, solo, precopulatory display in
front of the female and then mates with her. The two or three
males do not seem to be brothers, and Foster believes that the
benefit to the subordinate male comes not through kin selec-
tion but because the subordinate is younger, will eventually
inherit the display site, and will then become the dominant
member of the new pair. The subordinate is thus a symbiotic
apprentice, and is simply polishing his technique against the
day when he will come into his own.
I! is very hard to watch these displays and not try to imagine
what purpose they serve and why they evolved. So far, the
explanation that seems to have satisfied those ornithologists
that have studied the manakins directly is that two males can,
Male Society-the Society of Competition / 97
yields considerably.) Instead males compete with each other
for the available females.
Such a competition might be organized in several ways. The
CHAPTER most direct is simply sequestering the female; physically re-
x
MALE SOCIETY-
moving her from the attentions of other males. One example
of this kind of competition was studied in a species of sand bee
(Cent,;s pallida) by the members of a zoology class at Arizona
State University. The males of this desert dweller precede the
females in hatching out of the soil by a few days. The females
seem to dig upward and then pause just under the surface. The
THE SOCIETY male bees cruise "in rapid, sinuous flight" about an inch over
the desert. They seem to be able to sense alterations in the
OF COMPETITION pattern of odors given off by the sand and often drop to the
ground and walk about briefly, sweeping the soil with their
antennae. Then they either take off again or begin gnawing
and digging their way through the hard, sun-baked surface.
IF ONE WERE BUILDING A MYTH AROUND THE NATURE OF
Sometimes a male will dig down to a female in less than one
males, the center of the drama would be the moment when
and a half minutes; in other cases, he might need twenty. The
females took over the reproductive cycle, monopolized it, and
average excavation took six.
left males nothing to do but compete for their favor. When
When the male uncovers a female he begins to court her.
that happened females effectively emerged in control of male
This involves . . .
evolution, for it was only those males that met their terms and
danced to their tune that were able to reproduce. Conceivably . . . complex, rhythmic movements of the legs, abdomen, and
this need not have happened; had the males organized them- antennae of the male and is associated with a low soft rattling
selves, and agreed to ignore all the females, then eventually auditory component, perhaps produced by the female. Males
the females would have had to come looking for them. They vigorously stroked the sides of their partners with their middle
might thus have gotten the females to do all the work, from and hindlegs in a rhythmic fashion averaging about 1.3 strokes
per second. . . . At the same time . . . the male's abdomen
accumulating the protein to arranging the mating (though ac-
tapped the upper surface of the female's abdomen while the
tually if the males really had tried a trick like that the females
males antennae moved down along the female's antennae... .'
might just have evolved a bisexual life-style and dispensed with
males altogether). This courting behavior begins in the excavation pit but is
,.' " But in reality gender solidarity was never an option; sexual usually interrupted so that the couple can fly to some nearby
. (' ) creatures, as pointed out earlier, have an individualistic, anar- trees or shrubs; there courtship is resumed and at some point
,\\~ ,~ ~histic bent and seldom engage in compacts that entail sacrific- the female allows copulation to take place. The courting se-
V" \- mg for the common good. (For example, there is no known case quence takes only four minutes or so altogether.
/". •.' r of a predator species-humans perhaps aside- successfully The females mate only once and then flyaway ; the males
~I d'
. I ~. ~ a optmg a quota system, even though these can increase prey remain, cruising rapidly over the surface, looking for female
~.J ~tf '"
,u' -' ~ (1'"\.1 ,
98 I WHY MALES EXIST Male Society-the Society of Competition I 99
spoor. An intense male-male competition builds up rapidly. about one meter apart, on the margins of the regions where the
Digging males are often attacked by other males seeking to females are emerging, near flowering shrubs and trees, and
supplant them. hover, looking upward. These males are smaller than the dig-
gers and never make aggressive, physical contact with other
Digging males defend their sites vigorously. When ap-
proached and touched by an intruder, the site owner will elevate male sand bees. Almost certainly they are waiting to spy fe-
his body (first backing out of the hole if it is one cm or so deep) males that have escaped the attentions of the diggers; in experi-
and kick at his opponent. If the other bee does not leave, the ments involving the release of females such females were
digger will turn to face his antagonist and may then lunge for- chased and "captured" in flight. The biologists believe that
ward. If the potential usurper stands his ground, the two will darters must have been doing the chasing, since the diggers
then usually rear up on their hind legs while facing one an- seem to pay all their attention to the ground.
other. . . . If one bee is smaller than the other, he is likely to A direct, scrambling competition, in which females are
topple over backward and may leave promptly thereafter. Al- fought over one at a time, is common in insects, but it is cer-
ternatively, the two may grasp one another and grapple violently, tainly not restricted to them. The common garter snake ~ften
wrestling and twisting over the ground . . . until one manages overwinters in large aggregations. The males wake from hIber-
to break away and escape. nation first, crawl out of the cave or hollow, and then await,
On the mornings of May 14-17, 1975, at the Saguaro Lake
as a group, the females. The females wake over a range of
area, 50 records were made of activities at digging sites. . . . On
43 of the 50 records, a male was forced to interrupt his digging several days and straggle out a few at a time. Each is courted
to repel an intruder by kicking, lunging, or rearing up at his by dozens, hundreds of males. Courtship in garter snakes in-
opponent. A total of 393 such interruptions were noted or an volves a physical kneading of the female by the male; he rubs
average of 1.5 for every minute of digging. . . . Because the his head up and down over her back. A garter female, there-
average time required to dig down to a female is about 6 minutes, fore, may find herself surrounded by a great ,?any males ~I
males usually find it necessary to defend their digging sites re- trying simultaneously to massage her. After. a lI.me sh~ a~ml~s
peatedly. . . . (Of the 50 sites and 393 attempts there were one of that number; a pheromone announcmg mtromlsslOn IS
only 21 successful takeovers. In a second study area 10 digging released (it may be a mixture of substances produced by both
sites were watched and four successful takeovers were seen.)< sexes) and the mating ball dissolves.
The game, of course, is not over when the female is uncov- A last example of direct competition for individual females
ered. Intruders are likely to challenge a successful excavator might be the spawning practises of salmon. The female first
as soon as a female appears, to attempt to dislodge him during builds the redd, or egg-laying site; then, according to some
courtship, to interfere with his flight to the bushes, and to dis- observations made in 1934:
rupt his attempts at copulation. . . . she selects a favored male and will aid him in chasing
The female's response to all this scrapping and brawling is away other amorous males, although she will not go far from the
predictable enough: she flies away from it. If a male is dis- redd. In making her choice she favors the large males. . . . The
tracted or dislodged by an intruder once the female has role of favored male is not secure, since he may be supplanted
emerged, he might lose her regardless of his success vis-a-vis at any time during the season, day, or hour. ~en there is a
his competitor. The intensity of the fighting among the diggers surplus of males on the spawning grounds, c~l~mg males ~re
(and the females' avoidance of it) makes possible a second constantly shifting from female to female, awaltmg the cructal
male strategy, that of being a darter. Darters station themselves moment when they may share in the fertilization of the eggs.
100 / WHY MALES EXIST Male Society-the Society of Competition / 101
Within a period of five hours three different males may have previous set of males and usually manage to last for two to
been observed to occupy the position of favored lover, the larger three years before being driven out .in tum. .
cruising males driving off their smaller rivals. . . . When Another, exceptionally well-studIed example IS that of the
salmon are numerous on the spawning grounds, particularly at yellow-bellied marmot, a chunky, squirrel-like creature known
night, the water is kept in constant turmoil by the activities of for its ability to live at high altitudes. Marmots are one of t~e
the males chasing invaders from their chosen females. . . ,1.
more social of the rodents. Like prairie dogs (the most SOCial
A very common form of male competition is establishing rodent) they live in permanent colonies laid out over several
territories-areas or resources to which receptive females will acres and interconnected by an intricate series of home bur-
be attracted and from which males try to drive each other rows secondary or refuge burrows, and trails. Each colony
away. The competition is for the territories, not for the females is co:Oposed of two or more females and a male. (Prairie dog
directly, though there is sometimes an element of this, too. The colonies are really supercolonies, made up of many such
males of many species of insects, fish, amphibians, and reptiles families, all of whom will join to conduct a group defense of
struggle over control of "ovipositing" or egg-laying sites upon their common territory against outsiders and predators.)
which, once control is established, they wait for females to ar- Marmots hibernate seven months out of the year; they
rive. The dragonfly mating system is a classic instance of this. emerge in May and stay acti.ve until early or ~i~-September.
The females lay their eggs in lakes. The females of each species Happily this corresponds nicely WIth the actiVIty :ycle . ~f
-and sometimes different kinds of females within the same most college students and professors as well, and thIS feh~l
species-have distinct preferences among the variety of tex- tous symmetry has given us an intimate acquaint~nce wl.th
tures (mud clumps, algal and other vegetation mats, sticks and marmot society. It echoes many of the features of hon SOCIal
logs, and floating objects of various kinds) a lake offers. The biology. The females are more likely than not to be the
males usually appear first, fight over the sites that females of daughters of marmots that lived in that colony before them;
their kind of species will find attractive, and then wait for the male comes from further away, is not related to the fe-
them. Similarly, African antelope such as the sable, the impala, males and is usually turned out after two to three years by a
and the waterbuck contend over fractions of the range on succe~sor male. The males spend most of their time on the
which females forage. Males mate with those females that hap- alert for challenges to their tenancy. Kenneth Armitage, a
pen to become receptive in the area he controls. University of Kansas zoologist who has done more than any-
Most male mammals compete over "residency rights"-the one else to uncover and relate the intricacies of marmot so-
right to stay near a group of females that will, at some point, ciety, has written:
come into estrus. A famous example is lions. The core of
. . . The most striking characteristic of male adult behavior
lion sociality is the pride, more specifically, the females of
is its conspicuousness. As a colonial male moves around a lo-
the pride. These are a related group (mothers, daughters, cality, he carries his tail in an arc extending abo~e and to ~he
aunts, nieces, cousins, and sisters) of a half dozen or more rear of his body. The tail is waved back and for:h In a behavlO.r
lions, all of whom live together in a stable society in generally described as flagging. . . . Flagging is so eastly seen that It
the same area for long periods of time (a lioness might live for must serve to advertise the male's presence.-
eighteen years) . A pride usually has two males as well. These
are often brothers, but from another unrelated pride. They Males either survey their territories from one or two look-
win their right to live with the females by driving out the points or patrol them throughout the morning. Flagging is
directed at transient males that are not prepared to fight. Ad- opponent feel like a stranger, or at least less at home. Such
vertisement allows both parties to avoid the stress of a direct odors serve the same purpose as strutting and swelling. They
challenge. Sometimes a real challenge ;s made, though, and amplify the presence of their generator, or generatrix, and
open fights break out. Armitage was lucky enough to witness make his or her identity more pervasive. These odors, phero-
one of these: mones, are also used to control territory without physically
occupying it; they serve the same purpose as birdsongs, or
16 June 1968. 402 (the identifying number of the male) by
our system of property rights. Marmot 355, one might note
the upper cabin. 355 (the resident) comes up past the wall. Both
flagging and moving about. Much circling; first one advances, in this connection, was challenged only on those portions of
then the other. Each rubs head alongside bricks, etc., in the his extensive range that he visited least. He was never tested
yard. 355 returns to the wall and 402 follows and marks bricks on that area where he actually lived, patrolled most often,
at the wall, then retreats to cabin as 355 follows . More circling and where, presumably, the sense (and scent) of his presence
and flagging. Each appears to expose the anal region to the was strongest.
other. 355 starts down bank past wall and 402 follows. Suddenly A third form of male-male competition-known in several
402 jumps on 355 and vigorous wrestling follows . They appear species of insects, about thirty kinds of birds, some fish and
to lock jaws. 402 seems dominant, then 355. 402 broke off and frogs, and a handful of mammalian species--begins with
ran and 355 followed. 402 entered burrow under cabin porch what seems to be a statement of male organization. The
and 355 remains at entrance, jumping and moving around and males congregate and, acting collectively, pull the females in
rubs side of head on boards above burrow entrance, then lies from the surrounding area. Only when the females appear do
stretched out on board, then moves off.
they compete, usually through displays. One of the most im-
The background of this particular blow-by-blow was that pressive examples is found among the East Asian fireflies.
355 was defending a combined territory, one which had Enormous numbers of males assemble in hundred-yard
"traditionally" been three separate male ranges. He did this stretches of mangrove trees at night along river banks.
successfully, despite repeated challenges, for four years, which "Imagine a tree thirty-five to forty feet high thickly covered
is considerably longer than the average male residency in even with small ovate leaves," an American biologist, Hugh M.
single territories (two and a half years) . Marmot 402 re- Smith, once wrote of this phenomenon, "apparently with a
mained in the area despite losing this fight. He was trapped firefly on every leaf and all the fireflies flashing in perfect
by Armitage's team the following year and introduced, as an unison at the rate of about three times in two seconds, the
experiment, into a second colony area. He left, and the next tree being in complete darkness between flashes. . . •
year, 1970, turned up in a third area where the resident male Imagine a tenth of a mile of river front with an unbroken
had died. Here he was finally able to settle in with a group line of trees with fireflies on every leaf all flashing in syn-
of females of his own. chronism, the insects on the trees at the ends of the line acting
One of the more important elements of this fight is invisible in perfect unison with those between. . . ." 2.
to humans; 355 and 402 were almost certainly "shouting" at Biologists call these male mating aggregations lek systems.
each other over the olfactory channel. The head-rubbing, the The lek itself is the area, usually a very small part of the
marking, the mutual exposure of the anal regions, all are habitat, that is used, often year after year, for mating displays.
probably connected with an effort to make the battlefield The fidelity of the creatures using the lek can be remarkable.
smell like one's own homeground and therefore make the One population of ruffs in Britain continued displaying on its
traditional spot even after a road was built over it. The last were more frequent. . . . Typically, the pursuer trotted "de-
surviving heath hen in Martha's Vineyard, Massachusetts, liberately" toward the pursued male with head low, ears back,
became the object of some local sentiment by persisting in and horns flattened until the latter either left or was chased from
returning to the display grounds of her species, year after the area. The pursuer followed for a few meters and then pulled
year, and waiting fruitlessly for the booming, whooping, vocal up abruptly in a head-up display with vigorous head-shaking.
displays she no doubt remembered from her chickhood. [When a female entered a male's territory] he typically ran
When breeding time arrives, the local males migrate to the up to and around the female, trying to prevent her escape with-
lek and crowd into a number of small, adjacent territories; out physical contact. If she left the territory, the male's chase
from there they flash, whoop, boom, crackle, puff, flutter, and ended abruptly in a display, thus allowing the next male to take
generally transform themselves into as dramatic and eye- over and so on in relay until the female either chose to remain
within a male's territory or left the lek. Males entering a lek
catching a specimen as possible. The females wander around
were often chased successively in the same manner as if the lek
the lek, examining the various candidates. As a rule they end occupants were an elite "corporate body" defending the lek as
up all making the same selections. Usually only a tiny fraction a unit.
of the males successfully mate; these mate with almost all
the females. An example of a lek system in mammals might When females did stop within the lek, Schuster notes,
be that of the lechwe antelope (Kobus leche Gray) of Cen- usually between ten and twenty would be tightly clustered
tral Africa. Richard H. Schuster, of the University of Zambia, around one or two males.
has described their display. During rutting he found a number These three categories of male-male competition-scram-
of circular areas, about half a kilometer in diameter, within bling for females one at a time, monopolizing resources that
which fifty to one hundred males, spaced about fifteen meters females will approach or areas they will travel through, and \
apart, were displaying:
displaying to them in aggregations-often borrow elements
The males rarely grazed, but instead stood in an exaggerated from each other and, even as a whole, do not begin to exhaust
pose with head held high, legs prancing, tail wagging vigorously, the possibilities. There is a bug (Xylocaris maculipennis) ,
and penis often erect. . . . displaying is enhanced by features which appears to be able to insert its own sperm in the sperm
present only in the larger adult male-lyrate horns (lyre like ) duct of other males, \\!ho then use it during copulation instead
averaging seventy-two centimeters (two and a half feet) along of their own. And then there is a parasitic worm (Monilifor-
the front curve and solid black markings on the fore- and hind- mis dubius), the males of which, after they mate, have the
legs, with the foreleg patches extending up to conspicuous
practise of sealing off the female's genital tract with a con-
shoulder markings. [They also tear] at the ground with horns.
The head is swung vigorously from side to side, causing tufts gealing secretion. This presumably prevents other males from
of grass to be flung high into the air and often draped on the copulating with the female and competing with the first
horns and neck. male's sperm. Another possibility is that the secretion helps
. . . Lechwe leks were notable for the almost continual oc- prevent the male's sperm from leaking out. There is nothing
currence of male-to-male interactions between territorial occu- Unusual about mating plugs; they are found in a great many
pants, conveying an atmosphere that was highly charged and insects, reptiles, and rodents. What seems unique about this
unstable. The movement of a male or a female almost anywhere worm is that some males have been found with their genitals
was likely to set off a chain reaction of chases and fights . Chases sealed up. The investigators believe that given the specific
106 / WHY MALES EXIST Male Society-the Society of Competition / 107 "t
conditions under which this worm mates, it might well have Mortal battles between males are not common, though they f
been adaptive for males to take each other out of the mating do occur. A weak~ue not want to pick a fight he
pool by walling off their competitor's genital regions.' would be likely to lose; nor would a stronger male be selected
The list of devices through which males compete with each to risk a wound that would make his victory pointless. A
other is enormous. The males of some species, after mating period of symbolic conflict, of "showing off," is therefore
with a female, paint her with repellent, or at least antiattrac- adaptive for both parties. These are "swagger matches," in
tant, pheromones to discourage other males. In one fly species which each male attempts to demonstrate to the other that
(lohannseniella nitida) the male wedges into the female's his combative equipment, innate ferocity, agility, raw power,
tract and plugs it with his body. His genitals lock in place. and endurance are all so overwhelming that no one but a
Eventually the female breaks off the parts of his body that fool would try to match them. One of the more common \
are removable, but his genitalia remain. A common com- forms of symbolic conflict is moving air by roaring or bellow-
petitive strategy is a sort of pseudotransvestism. Females often ing,· but males also commonly blow themselves up to look
have a characteristic color and/ or behavior pattern that re- as large as possible, violently attack objects in the immediate
duces the hostility of males by serving as a gender cue. The area, and feint and dart and charge and shove without getting
males of a number of species imitate this behavior or show these mortally serious. All during these displays both antagonists
colors, subvert the defensive hostility of the dominant male, are calculating their chances in a serious fight. Here is an ex-
lurk about his territory, and sneak matings at an opportune ample, a challenge brought by one musk-ox (in Alberta,
moment. Sometimes males combine to compete. Some species Canada) against a "harem" owning bull:
of frogs call in duos, or trios, or even in quartets (within a
[The recording biologists were attracted to the scene by]
larger lek display); each member of the group sings a different
numerous throaty, Iionlike roars. . . . The fight itself was
part. If one is removed the others stop singing and begin to initiated by the challenger who charged the harem bull with
search, apparently looking for another partner with the right lowered head from a distance of about ten meters. The harem
range. This searching will stop if a new "partner" is reintro- bull stood his ground so tbat both animals sustained the brunt
duced by playing a tape of the old partner's song. In a popu- of the impact on the bosses of their horns. They maintained
lation of wild turkeys observed in southwestern Texas, two- contact for a few secondsafter the clash and pushed vigorously
or three-member bands of male turkeys (brothers) courted against each other. On the cessation of contact the harem bull
females synchronously, strutting, fantailing, and pinwheeling swung his head rapidly from side to side as he backed up and in
about her with the precision of a drill team. Juvenile males doing so apparently struck the challenger lightly on the sides of
in some tropical-fish species, among them the common platy- the face and neck with the tips of his horns. Both combatants
fish / guppy, will delay their maturation if kept in a tank with then backed away from each other some ten meters while swing-
ing their heads slowly from side to side, then turned parallel to
an adult male. One interpretation is that these males are able
one another and "strutted" in a stiff-legged gait. The harem bull
to use their maturation cycle as a competitive instrument. then turned his back on the challenger and "thrashed" a clump
They stop growing when they reach maturity; larger males
probably are more successful. Therefore, the theory runs, the • Tacitus said of German war chants: "By the rendering of this they not only
juveniles deliberately retard their maturation so as to give kindle their courage, but merely by listening to the sound they can forecast \
them the best chance of growing larger and beating the neigh- the issue of an approaching engagement. For they either terrify their foes
Or themselves become frightened, according to the character of the noise
borhood dominant. they make upon the battlefield. . . .It
108 / WHY MALES EXIST Male Society-the Society 0/ Competition / 109
of willows with his horns. Thereupon, the challenger turned males is to lurk around a dominant's females and steal
away from the harem bull, strutted a short distance, and sud- them when he is distracted by a fight. He calls this the
denly broke into a run which precipitated a chase of about one "sneaky fucker strategy". (Clutton-Brock believes that 20
kilometer. percent of the red stags are permanently injured anyway in
fights over their four years of reproductive life.) This tech-
The naturalists who watched this challenge, Paul Wilkinson nique of assessing combat potential indirectly has even been
and Christopher Shank, explain that the head-swinging is traced back to the dinosaurs. The hadrosaurs had long, hol-
likely to be a reenactment of one of the basic tactics of musk- low crests, the chambers of which connected to the nasal
ox combat, which is stunning the opponent with a hard charge passages. One plausible suggestion as to the purpose of these
to the head, slipping by his defenses while he is dazed, and structures is that they were powerful resonators through
then stabbing up into his side. Obviously enough informa- which males thundered at each other, just the way elephant
tion was exchanged during the interaction described here for seals do today.
the challenger to decide against a serious attack. Sometimes The whole thrust of the system is to work toward shorter \
the decision can go the other way, of course: Wilkinson and male lifetimes. This is not just because of the misadventures
Shank estimate that between 5 and 10 percent of the musk -ox of combat; a male's mating success rises and falls very rapidly
1 males in the herd they were watching died from direct bat- as he reaches and passes his prime condition. A male that
I
tles during the 1973 rut. lived for a long time in a slightly less-than-prime condition
Tim Clutton-Brock, of King's College Research Centre would father very few offspring, because during any single
in Cambridge, was able to experiment directly with the phe- season he would be kept from mating by the males who were
nomenon. He had been watching the swagger matches of red then at their peak. A male who instead trades off long-run
deer stags and discovered that the rate of roars (among other survival for a more intense mobilization of his energies over
factors) was an excellent predictor of the outcome of the the short run, who throws his all into the fray with no thought
match. The stag that roared fastest carried the day. Clutton- for the morrow, will, in many common mating systems, be
Brock made three tapes of this roaring: one at two and a half more successful and, Darwinism predicts, will come to define
roars per minute, a second at five per minute, and a third at the gender. It is the winners that control the system; losers
ten per minute, which is much faster than any mortal stag have no voice. The males that make these arrangements work
could ever produce. (A typical natural rate is six roars per for them will be the ones to mate; it matters not at all how
minute.) He then planted loudspeakers in the rutting area much havoc any given mating system might have wrought
and played these three tapes when stags with females came among the losers. Nor will the females ever be selected to
by. The two-and-a-half-minute tape produced little response modify their mating behavior so as to make things easier
from the dominants. When the stag heard the five-minute for males, at least not unless the carnage rises to such a point
tape he herded his hinds together and threatened the loud- that they have to wait an inconvenient length of time to be
speakers. And whe~eard the ten-minute tape, "he leaped fertilized.
to his feet and looked extremely worried." Red stags, in-
cidentally, have a special motivation to develop ways of
resolving a challenge without entering into direct battle. Clut-
ton-Brock has found that a secondary mating strategy for
Female Influences on Male Society / 111
Lions are an example of creatures tha~e ... male com- \ 1
petition in this way. The lionesses of a pr~me into and

go out of a short (two-to-three day) period ~f heat simul-
taneously. During this time each lioness requires enormous
CHAPTER
amounts of energy for each effective fertilization-often mat-
ing every fifteen minutes over ~his period. It has b,:en written
XI that the males ejaculate each time (though how eVidence was
gathered on this point I cannot im~gine), ~~t ~ost matings
do not result in cubs. Each productIve fertilization therefore
takes a lot out of a lion. This feature of lioness's reproductive
FEMALE INFLUENCES physiology is thought to have resulted from selection to les.sen
ON MALE SOCIETY the amount of competition between the males of a pnde.
Wh.en a new set of male lions invades and takes over a pride,
they kill the c~ gathered by the previous set of males. Fe-
ihaleHlrerEfore ought to have an interest in reducing the rate
IF FEMALES WERE RESPONSIBLE FOR THE ORIGIN OF MALES of turnovers, and, since two lions can put up a bette~ defen.se
(by expropriating the reproductive cycle) and their further than one, of retaining two males that are cooperatively diS-
development (by picking just those males that offered the best posed toward each other. Competition between the males of
service and the highest quality), it seems natural to ask a pride exists, but, compared with that of other male mammals,
whether they might also have designed the nature of male is weak. These long, exhausting copulations surely help to-
society. In other words, do females control the intensity of ward this end. By the time a male has finished fertilizing the
male competition, and if so, to what degree? three or so lionesses that are his norm, he would probably
Certainly the instruments for that control lie in their hands. be too exhausted to compete for the other three, even if the
If the females bunch together during the breeding season, second male hadn't already fertilized them, or the females
then an individual male can defend more mates than he could weren't already passing out of estrus.
if he had to travel around to females dispersed throughout the Given this degree of potential control, it is interestin~ ~hat
habitat. So when females group together, for whatever reason, females, by and large, do nothing to lessen male competl~lon.
they make male competition more stressful, demanding, and The pups of elephant seal cows, for instance, are so~etlmes
violent by raising the stakes. If the females of a population crushed under charging bulls. The seal females might be
clock their cycle in some regular, predictable way, then a dom- expected to defend their pups by spacing themselves out, so
inant male will be able to use his time most efficiently, and that the males have to devote some time and energy to travel,
this will increase the importance of being dominant in the or they might cluster in groups of hundreds or tho~sands,
first place. in which case the competition would become too taxmg for
Or if all the females in a group become receptive at once, any bull, no matter how formidable. Instead they gr~u~
then a dominant would have great difficulty in controlling the (usually), in nice, defensible units of a few dozen. ~y IS It
situation; by the time he was finished with his first female,
the game would be over for the year.
that they cluster in just those patterns that seem to ~nve male
competition to its most intense level? (The answer IS not that
(
112 / WHY MALES EXIST Female Influences on Male Society / 113
the males impose the organization. It used to be thought that and sometimes their purpose is easy to understand. Female
the males herded the females , and it is true that they can be toads (B ufo hufo) seem to use incitement in order to acquire
seen trying; but the females are both numerous and agile and the male most likely to fertilize more of her eggs. Female
in fact move relatively freely from "harem" to "harem". Males toads have reasons for strongly preferring large males. They
l almost never succeed in imposing control over groups of

females in nature; the famous example of the hamadryas ba-
boon males is virtually unique.)
Female behavior in nature often seems to enhance male
release their eggs into the environment unfertilized and de-
pend on the males (who clasp themselves onto the female's
back) to cover the eggs with sperm. Only a large male can
both maintain his lock on the female's back (he grips her
competitiveness rather than reduce it. Female garter snakes under the arms and around the chest) and be physically ca-
appear to insure that they will be mobbed by the largest pable of releasing his sperm over all her eggs. The smaller
number of males by spreading the dates when they emerge the male in proportion to the female, the lower the percentage
from hibernation over several days. Sand-bee females dig of fertilized eggs.
toward the sand surface and then stop. This induces males However, there are not that many large males (Bufo fe-
to dig down toward them, and during those excavations, the males are larger than males *), and large females often end
males are repeatedly challenged (at a rate of four challenges up with smaller males getting a lock on them than they would
per average excavation). It is very common to see females like. Two Oxford zoologists, Davies and Halliday, upon
appear to delay mating until a number of males have been looking more closely into the matter, found that while large
gathered together first. H. T. Gier gives an example from the females are often seen carrying small males before spawning,
life of the American coyote: during the act itself large females and large males were found
to be paired. The zoologists made some experiments that es-
A coyote family has its inception in midwinter when a female
comes into estrus and attracts one or more sexually active tablished that a large male can dislodge a small one from a
males. . . . It appears that all the reactive, unattached males
• It might be pointed out that males in nature are usually smaller than
within an attractive female's territory join the parade and follow females. There are very few invertebrate species in which the males are not
the female for days. I have seen as many as seven males follow- smaller than females (this decides the question of overall frequency on the
ing one estrous female. . . . The males follow for as long as spot). Species of fish in which the males are larger than the .females p~ob
ab ly number less than a third of the total. l arger-m ale species are a hule
four weeks. . . . Copulation occurred when the female stopped, more common among reptiles and amphibians. They might constitu!e ,a
nuzzled a male, then positioned herself to that male and lifted majority of the bird species and certainly do of the mammals, but even wlthm
her tail. . . . From observations in the field and on penned the mammal class, larger females are not rare . A recent study 119 sh~ws
that larger-female species occur in 30 of the 122 families o~ mam!11a1 speCies,
animals, I am forced to the conclusion that the female makes ranging from a family of bats to three families of whales, mcludmg the blue
the choice as to which male will be allowed to mate. Whale, which means the largest animal on earth is a female. Larger-female
species are also common among the few species of monogamous mammals.
Observations like these suggest that in some cases females One reason why males tend to be smaller, at least in the smaller animals, '-
is that they become reproductively functional at ~ younger age. S~erm--t::
might have some reason to foment an even more intense level takes less time to build than eggs . The old observation about male spiders
of male competition than would have existed. The most direct hatch ing first and leaving the egg case before the females might be ex-
evidence on this point is incitement, instances when females plained best not as a defense against incest, but just because the males are
ready to go earlier, Also, where ther~ are disadvantages to bein,g large
can be seen, or heard, actually stirring up one male against (clumsiness, conspicuousness, bulk in birds), males are freer to aVOid them
another. Examples of female incitement are fairly common, because sperm is so much smaller than eggs.
114 / WHY MALES EXIST Female Influences on Male Society / l1S
female's back. They point out that large males have a dis- d returns from the fray thoroughly beaten, it is quite fre-
tinctive caII (the bigger the male the bigger his voice box and ~~ent that the seemingly implacable female will promptly reject
the more basso his call will be), and conclude: her mate and begin to court the victor, regardless of what spe-
. . . male-male competition is the mechanism by which the cies it may bel
change in pairing from prespawning to spawning comes about. And finally, I would like to pass on this report, made .by
. . . Because it is the fema le who is in control of locomotion of an amateur arachnidologist in West Virginia of the behaVIOr
the pair (her legs are free for swimming) it seems likely that she of a local web-spinning spider (Verrucosa arenata):
will be able to influence whether male-male competition takes
place or not. If she has a suitable mate she may swim away One male was found four centimeters from the retreat of the
from other males in order to avoid interference. If she has been female. Another male crawled up the upper foundation thread
grabbed by an unsuitable male then we suggest that one strategy toward the retreat, periodically giving a series of four. to fi~e
she could use would be to swim over to where there are other jerks on the thread. The female, resting in .the hub dunng thiS
males and thus invite male-male competition. time, responded each time with four to five Jerks. When the sec-
ond male reached the vicinity of the retreat, the males exc~an~ed
Large males would prefer to mate with a large female if jerks, approached each other, and combat occ~rre? (by thl~ tl~e
possible, because large females lay many more eggs. the female had moved to her retreat), resultmg m the eViction
As a rule the rationale of female incitement is seldom so of the first male."
obvious. Yet it is quite common. In many squirrels estrus is
announced by the female with a screech or a rattle, or a It looks as though the female recruited the second male
pheromone discharge, which brings all the males in the area to fight with the first. .
after her in a rush. "If she stops vocalizing for a while," writes The species in which female incitement is best known ~s
one zoologist of the African bush squirrel, "a male might the elephant seal. George Bartholomew, who wr~te the claSSIC
begin to move away, but as soon as the female calls again, he study of these animals in the early 195?~, speclficaIIy n~ted
will turn around immediately and move toward her." 148 Sim- the intimate connection between competillon and copulation.
The dominant males "rarely engage spontaneously in copula-
ilar behavior (of females inciting pursuit by a number of
tion," he wrote. "Instead their sexual activities usually devel-
males) has been seen in white-tailed deer, bison, rats, a land
crab, mountain sheep, Pacific bonito (when ready to spawn oped as an aftermath of the efforts of one or m~re subordinate
the female swims in an exaggerated, wobbling motion that males to copulate with females . . . over whlc.h one of the
attracts males) , and a number of birds, including the pintail harem masters maintained dominance. CopulatIOn appeared
duck, winter wren, and sanderling (the females of which to be used as an expression of dominance rather than an end
in itself."
initiate aerial chases). Courtship among the shelducks and
sheldgeese (water fowl) takes the form of the male's alter- He illustrates with the following example:
nately directing sexual displays to his intended mate and threat On the hauling ground at West Anchorage, at low tide.in the
displays in some other direction. Paul Johnsgard writes: middle of the afternoon, a small female not more than SIX and
a half feet long left the other females and headed down the
Female shelducks and sheldgeese are exceedingly aggressive beach toward the sea. As usual the female's departure caused
birds and usually Incite [Johnsgard's emphasis] their males to no response from the male dominant over the part of the herd in
attack almost every animate object. If the male responds blindly which she had been lying.
When the small female had crawled about thirty feet, she After a few minutes of this the female "acquiesces"; some-
passed one of the subordinate males; the male remained motion- times even arching her lumbar region to make her vulva more
less until she had passed, then roused himself, turned, overtook accessible. Bartholomew's observations suggest that the female
her before she had gone another eight feet, pinned her to the controls the passage of sperm into her body:
ground with the weight of his body, and after not more than five
seconds began to copulate with her. . . . as soon as his penis is inserted the male becomes almost
Copulation had been under way less than fifteen seconds when completely passive. He lies half on his side and half on his belly,
the male dominant over the part of the herd from which the eyes closed, pelvis thrust forward, and one flipper holding the
female had departed discovered the pair's activities. This par- female. For the most part the two animals lie almost motionless,
ticular dominant male had so far during the day shown no sign sometimes with their bodies at a marked angle to each other.
of sexual interest in any of the many females available to him, . . . During the last half of the copulation the female assumes
but now, after rearing up and vocalizing once with great force; the active role. Mild undulations pass slowly through the
he moved at top speed toward the copulating pair. posterior part of her lower trunk, and she flexes and extends
The subordinate male, apparently unaware that the dominant her hind flippers gently. Often she performs a series of slight
male's vocal challenge had been directed at him, did not per- dorso-ventral flexions with the posterior part of the body which
ceive the dominant's approach until the latter was only five or slide the vagina back and forth over the penis. . . . Copulation
six feet away. The realization that he was being charged so dis- lasts three to seven minutes and is almost invariably terminated
turbed the copulating male that he instantly headed for the water by the male.
as fast as he could go, without even bothering to disengage him~
self from the female. Recently these "protests" have been studied intensively by
The female, whose back had been bent almost double by the Cathleen Cox and Burney J. Le Boeuf. They found that males
subordinate male's hasty departure, did not move away after mounting estrous females are more than twice as likely to be
the male pulled free. As the dominant came abreast of her he driven away by other males when the female protests than
stopped abruptly, paused a few seconds watching the flight of when she remains silent. Thus the picture that emerges is that
the displaced male, and then promptly pinned the female down the females have a substantial degree of control over the fer-
and began to copulate with her. . . . The dominant male's tilization process, and that they use this control, at least in
sexual response appeared to be a direct result of the challenge part, to play males off against each other.
to his social position by another male and only secondarily a Why do they do this, if they do? What could be the point?
response to the female. Perhaps the single observation that can be made about the
During copulation, Bartholomew notes, the male has to range of ways one male is chosen out of the many that are
wrestle the female about for a short time; during this period called is that physical exertion is almost always involved, or
she often will bawl a loud "protest"-the word is Barthol- demanded. It might be that the female is interposing a test that
omew's-and flip her pelvis and hind flippers rapidly and prevents her mating with gross misfits, from pairing her genes
repeatedly from side to side in an arc. She may also flip sand with genes that are defective.
at the male and nip him on the neck. He seems to struggle to The case that fits this suggestion best is male competition
keep her quiet, pinning her down with his great bulk (males among those creatures in which the males have only one gene
weigh about three times more than females), clasping her with set instead of the usual two. A male of such a species has only
his flippers, biting her on the neck, and striking her with his one source of genetic information. If one of his genes is defec-
open jaws. tive he must rely on it, use it, and express it, regardless. Mating
among the social insects-a prime example of these one-gene- to the female, so tightly, in fact, that the female might be cut
set males-is just as strenuous as among the larger-bodied in two. Eventually the female allows the male to mate with her.
species we have been reviewing. In some cases a queen flies to After a few minutes he relaxes his grip on her thorax and,
great heights so that only the fastest, highest-flying males can while still hanging on, and with his organs still inserted, rolls
reach her; on others she might crawl along the ground, requir- over to her lower side where he massages her gaster (abdo-
ing the males to search for her over periods of as long as several men). (This might have something to do with sperm transport.)
weeks. A second male then catches hold of the female's thorax and,
Another kind of "test" is more familiar, relying on leklike while still more males tug at him, waits for the first to uncouple.
swarms of males all actively battling each other for access to Then the female begins to bite the gaster of the first male, who
females. An example might be the mating behavior of a seed- decouples, often with such speed that his organs are left cling-
eating harvester ant (Pogonomyrmex) that lives in the Ari- ing to the female's genitalia. The second male then copulates,
zona desert. In at least some sections of the desert there are six if he can, and is often followed by a third. Holldobler showed
Pogonomyrmex species living together. Each species has its that the females release an incitement pheromone from their
own mating site and its own time slot for visiting that site. poison glands which, if extracted and dropped into a cage of
(How all the nests of the same species in an area get to know males with no females present, will induce homosexual mount-
which site is theirs, how to get to it, and when to visit, is an ing.
interesting mystery. Bert Holldobler of Harvard has studied Thus whatever else mating activity accomplishes in these
this ant and reports that the sites in his study were flat stretches ants, it will surely exclude males with muscular or mechanical
of ground for two species and bushes and trees for two others. deficiencies. Perhaps the practise of making males from un-
To the entomologist the chosen sites seemed indistinguishable fertilized eggs, and therefore with only one gene set, evolved
from numberless others in the area, but, generation after gen- in the first place because of the benefits of giving a stress test
eration, each species' reproductives congregate in the same to the genes being passed on. (The model works best if we
spot, flying in from nests scattered all around the countryside.) assume a context of brother-sister matings; perhaps in isolated
The first males to arrive release a sweet odor, detectable to colonies.) In any case making males from unfertilized eggs is
humans, which attracts both the females and more males. fairly popular among the invertebrates; it has arisen five times
While waiting for the females to arrive these early males "run in the insects, once in the mites, and once in the rotifers. Sperm
about in a frenzied manner." As soon as each female alights also have only one gene set, of course, and something like the
she is immediately surrounded by three to ten males. "At the present argument has been made about those sperm that fail
height of the activity," Holldobler writes, "thousands of such during the race to the egg; that the egg, in effect, picks the
mating clusters carpeted the ground. As many as fifty clusters Sperm that suits it best. One researcher with a light touch was
could be found in one square meter." able to retrieve sperm that had ascended a female rabbit's
The first male to reach the female grasps her thorax with his genital tract; it was mixed with fresh sperm and reinserted into
mandibles and forelegs and tries to insert his organs. The fe- the uterus of a second female. Several aspects of the experi-
male twists her abdomen away from the probing organs, deny- mental design were thought to give an advantage to the fresh
ing them entrance. Other males grasp the first male and pull at sperm, yet the sperm that had already survived in the first rabbit
him, trying to tear him off the female's back, which they some- was a far more effective fertilizer. In other words, the ability
times succeed in doing. The first male reacts by clinging tightly of the sperm to endure the murderous world of the uterus
(murderous to a sperm: 99.999+ percent of them die there) garmani female is receptive, she perches on the exposed, lower
also says something about its ability to perform its fertilizing portion of a tree trunk, faces down toward the ground, and
function competently. elevates her rear slightly. If a male approaches her and is
One problem with the "stress-test" idea is that it only works accepted, the two enter into a copulation that can extend for
in any clear-cut way with those genes important to surviving as long as twenty-five minutes. The elite theory-applied in
the test. The mates of the Pogonomyrmex females will be this case by Robert Trivers-is that this behavior allows the
physically adequate, but how about mentally? Harvester ants females to bring three kinds of males into competition: large,
have to be good foragers; where does that get tested? Nonethe- dominant territory-holders; transient vagabonds; and small
less, all things considered, while the stress-test idea does not subordinate males that live surreptitiously at the borders of
~nswer every question that idle intellectuals might dream up, the dominants' territories. Of forty-nine matings observed,
It seems a sober and useful contribution. To state this hypoth- the score was: dominants, forty-four; vagabonds, three;
esis in summary form: A certain fraction of the male popula- and small subordinates, two. He believes that the females'
tion (say 5 percent to 10 percent) is assumed to be genetically public mating habits are responsible for this lopsided score,
defective. The females that drift into using their tools of ag- since by exhibiting themselves as they do they make it more
gregation, asynchrony, and sperm control to foster male com- likely that the dominant male, who is most likely to win any
petition mate less often with defectives, and prosper thereby. dominance encounter, will see them. If females profit from
They need take no other action, no evaluating, assaying, or mating with large males, because these males have proved
sampling. Once they've set up the basic conditions the males themselves best adapted to the conditions at hand, then this
will do the rest. sort of exhibitionism would have a sound evolutionary founda-
Still, there are other possibilities. Typically victory in these tion.
male-male encounters, including those incited by females, goes Cathleen Cox and Burney J . Le Boeuf have also applied
to the larger male. This might be an individual who has sur- this theory, in this case, to elephant seals. As noted earlier,
vived longer, or been more efficient at exploiting the territory, they discovered that the protest calls that seal females voice
or both. If any part of that superiority is inheritable, then during mating attempts act, whatever the motives of the par-
females might be selected to see that they mate with the largest ticipants, as incitement calls, since they double the chance that
male around. This might be called the adaptive elite theory. a second male will intervene and interrupt the attempt. Two
The suggestion is that male competition is useful to females, patterns emerged from a study of these calls. First, females
and therefore worth inciting, because it screens out the major- protested virtually all mounts at the beginning of their ap-
ity of merely adequate males in favor of a handful that are proximately week-long fertile period. (Females give birth to a
qualitatively superior in some way. single pup about six days after they arrive; the pup is nursed
Each male constitutes an experiment in which a different set for twenty-eight days and then weaned, at which point the
of genes is tested against the environment. A large male means female returns to the sea. The females mate over the last few
that the experiment was a success; his genes are therefore good days before they return.) But as the day of departure nears,
ones for females to mix with their own. This idea has been they protest less and less; by the last day a majority of mount
used to explain the peculiar practise that many species of attempts are not protested at all. Second, the mating attempts
tropic~l lizards (genus: Anolis) have of copulating in highly of young, small males were protested more often and more
COnspICUOUS places. To give a specific example, when an A. Vigorously. "When young, low-ranking males mounted a fe-
male," the authors write, "it was apparent from their shifty especially attractive mates because mortality among males is
eyes and nervous behavior that they were constantly monitor- high (about half the males of breeding age seem to die from
ing the movements of nearby, larger males and were afraid of one year to the next), and males that survive demonstrate
being attacked." At the very least these patterns show-if there valuable qualities by that fact alone.
we~e any doubts about it-that females can and do regulate The elephant seal females apparently can manipulate the
therr calls t~ some end. In the beginning of the estrus cycle, system in the opposite direction as well, toward the relaxation
the top·rankmg bull or bulls account for 90 percent or more of male competition. Most females--even those that copulated
of the matings.
repeatedly earlier-mate at the very end of their season, just as
The manner in wh!ch the females incite males to compete they leave the rookery and begin to swim out to sea. The reason
for them must be clarified [Cox and Le Boeuf write]. One can- they do this, Cox and Le Boeuf believe, is that the few males
~ot distinguish . wheth.er .females are simply protesting a copula- that monopolize breeding during the major part of the season
tion or attemptmg to mClte noncopulating males to intervene and copulate continually, both day and night, sometimes for hour
chase off a mounting male. From the observer's blind it looks after hour after hour. Male mammals need high concentrations
as. if protesting females simply do not want to copuiate, and of sperm to fertilize effectively; a human with "only" five
thIS may be the case. The important thing is . . . the effect of million sperm per milliliter of ejaculation has a very poor
her be?av!or on nearby males. A blatant, squawking, wriggling, chance of paternity. It is possible that not even so formidable
sand-fi~ppmg female with a prospective suitor on top of her
a creature as an alpha (top-ranking) bull seal can produce
strugghng to pm her down attracts the attention of all males in
the vicinity . . . [and] sets in motion a sequence of male sperm fast enough to satisfy the demands being made on that
movements. For example a male dominant to the mounter supply. Thus a female that had copulated, even repeatedly,
may issue a vocal threat sufficient to move the mounter from with an alpha male might not have been successfully fertilized .
the female. But before the aggressor can reach the female The last-moment matings can be understood as a fertilization
he is threatened and displaced by another male dominant to insurance-preferably "bought" from a male who has not
him. Several aggressive interactions involving other males may copulated at these high rates in the near past. The females
e~ue, resulting. in a considerable change in the spatial relation- therefore leave the harem bulls' sphere of influence and mate
shIps of males ID the area. Episodes like this usually end when with a peripheral male.
the most dominant male in the area gets close to the female and
prevents all other males from mounting her or he mounts her These males adopted the strategy of pursuing departing fe-
himself. . . . males. The male that copulated was usually a low-ranking male
If females did not protest copUlations, males would stilI com- relative to males in the harem and one who copulated infre-
pete for females and interfere with each other's copUlations. . . . quently, less than ten times during the entire breeding season.
The effect of.~ female's protesting behavior is to intensify male- . . . Only one out of every ten mounts directed to departing
ma!e competItIOn and augment its consequences. Her behavior females was protested. . . . Whereas alpha males were usually
actIvates the social hierarchy; it literally wakes up sleeping males the first male with whom a female copulated, in only three out
and prompts them to live up to their social positions. The result of twenty cases was he the last.
is that it is more difficult for young males to mate and the
breeding monopoly of a few adult males is increased. ' This seems to show that the females can control their rela-
tionShips with males through their control of the structure of
Cox and Le Boeuf believe that old, mature males might be male competition.
The adaptive elite theory crops up again and again. H. T. specific competencies rather than ecological adaptiveness or
Gier, whose observations on the coyote were quoted earlier, general physiological superiority. Robert Trivers has speculated
said that in the mating system of that species (which, the that the horns of male reindeer had been shaped so as to adver-
reader may recall, involved a female's leading a file of males tise an ability of metabolizing calcium. These horns, he points
around behind her for as much as a month before she made out, are not very effective as weapons. The sharp, knifelike
a choice) . .. horns of the mountain goat or the fistlike horns of the moun-
tain sheep both seem better suited to that end. Reindeer males
. . . Ovulation occurs two or three days before the end of occasionally get their horns so tangled up that the combatants
receptivity, so in most cases, elimination of the suitors, either starve to death, which does not suggest good weapon design.
by discouragement by stronger males, dissipation of stamina, or
Further, they seem most imposing when viewed from the side;
rejection by the bitch, has been effective in limiting the sire of
the pups to the strongest, most cunning male available. head-on their points and branches tend to fall into the same
planes and vanish. One would think that if these horns had
Perhaps the most extreme formulation of the theory is the something to do with weaponry, they would have been selected
suggestion of Amotz Zahavi of Tel Aviv University that there to look most impressive from the viewpoint of the opposing
exists a "handicap principle" in male evolution. He points out male, or head-on. Nor are they used against predators; in fact
that it is common to see males undertaking what appear to be they are shed just before those seasons, fall and winter, in
pointlessly grandiose adventures-the defense of a territory far which predator attacks must be most severe. They must be ex-
larger than any they might need for strictly bioenergetic pur- pensive to produce, and certainly add enormously to the bur-
poses, or (more subtly) the flaunting of bright colors or noise- dens of running (especially through low-hanging foliage!).
making in habitats where predators stalk. His suggestion is Trivers notes that the horns of these species become larger,
that females might have evolved to pick males who have suc- both absolutely and as a proportion of body weight, as we
cessfully proved their quality in a "swim-the-widest-river, look at larger and larger species, up to and including the elk,
climb-the-highest-mountain" kind of test. caribou, and moose. The young of all these animals are able
The handicap principle carries the idea of female leverage to run with their mothers shortly after birth (often in only a
to an extreme. It is one thing to force the males to compete few hours). Thus they cannot be the size of cubs or pups when
among themselves for access to females; no new adaptations born; they have to be large enough to keep up with a running
are needed to imagine that process beginning. The handicap deer, and must also have a developed capacity to support their
principle requires that a separate adaptation arise, the "handi- body weight over the range of demands imposed by hard run-
cap," and that it necessarily involve some of its bearers throw- ning. Skill at extracting and processing calcium is therefore
ing their lives away. All one can say is that the rewards to important to females since their daughters will have to be able
the survivors would have to be enormous; females would have to bring the bones of their embryos to a high state of develop-
to be interested in no other issues (like the conveniences of ment; the larger the species, the more intense this need will
where and when, or courting skill). And they would have to be be, and therefore, the more important it is for males to establish
predisposed to begin rewarding such reckless behavior as soon their competence on the matter. .
as it appeared, else surely so costly a trait would be abandoned, There is a third approach to this issue of female chOice,
even by males, very soon. Yet, who knows. incitement, and male competition. It is possible that females
There are variants of the genetic-elite theory that stress choose males purely because they are attractive, are socially
adapted, and that incitement is useful just because it allows a females mate they will pick according to their taste, and when
comparative examination of the candidates, like a line-up. In they give birth the exercise of that taste will have increased the
other words, perhaps in some species most or all of the males number of attractive males, who in the fourth generation will
around will, if given a chance, father offspring that will be further spread among females the genes for this mating cri-
roughly equivalent in their physiological quality and environ- terion, and so on. The system reciprocally accelerates itself,
mental competence. Where these offspring will differ will be and, on paper and in computers anyway, seems to show that if
in one point only: the sons of some of the males will be more there is no better idea around, females will rapidly be selected
attractive to females than the sons of other males. By this to winnow down their choices among the excess males by the
theory females will pick good-looking males for mates because assertion of aesthetic criteria alone. Peacocks come to mind as
if they do so, their sons will be more likely to be good-looking, an example of a species in which it looks as though the males
and therefore mate more often themselves. have become objects of art, pleasant to contemplate, defined
The reasoning goes as follows: Imagine a condition in which by and selected for aesthetic terms and functions alone, and
the females of a species are generally surrounded by a number having no economic function. (But it is also possible that long
of importunate candidates, all of whom are approximately tail feathers do communicate something about the physiolog-
equivalent in paternal value and with whom the females mate ical or ecological adaptiveness of the male. They certainly fit
at random. Then assume that one female develops a preference Zahavi's handicap theory aptly enough.) Birds that display
for males with long tail feathers and only mates with the "pret- in aggregations, or leks, often appear to be competing on
tiest" member, by this standard, of any group of candidates. aesthetic grounds. One naturalist wrote about the displays of a
The development of this preference neither adds to or subtracts European shore bird, the ruff Philomachus pugnax:
from her reproductive success and she enjoys whatever the Males with relatively high rates of copulation differ from other
norm is for the females of her species, generation, and region. males on the lek with respect to the development of their nuptial
In the second generation her daughters will inherit this prefer- plumage. On all leks observed, preferred males were charac-
ence and her sons will inherit longer tail feathers. Her daugh- terized by an optimal development of the nuptial plumage. . . .
ters will reproduce at the local norm, but her sons will do Thus it is likely that size and brilliance of the nuptial plumage
somewhat better: They will get both their normal allotment directly influence a female's choice. This conclusion is also sup-
of matings from the randomly mating females plus they will ported by the observations of Selous who noted that "hand-
have a competitive edge in attracting their sisters. Assuming some" males characterized by a full plumage were selected most
that inbreeding problems are either not severe, or, because the frequently by the females. 78
population is small and isolated, an equal trial for everyone,
the males with long tail feathers will leave more offspring than
the ordinary males. The attractive males have also been carry-
ing within themselves the genes predisposing females toward
long feathers-though unexpressed, of course, because they
are males. These genes now begin to show up in the daughters
of the third generation. The proportion of females in the pop-
ulation that prefer males with long tail feathers will also begin
to grow, riding the success of their fathers. When these
The Cost of Male Competition to Females I 129
bull should be selected to care for the pups of the males who
fertilized the female last year, and they don't. A more insidious
instance of how male-male competition can be destructive to a
CHAPTER female's interests is the practise of infanticide, and this is a
story worth developing at length.
XII The hanuman langur (Presby tis en tel/us) is a black-faced,

gray-furred monkey that ranges all across the Indian subcon-
tinent, from the Himalayas to the southern coastline. They
are "about the size of a springer spaniel," Sarah B1affer Hrdy,
THE COST OF who studied these primates for five years, writes, "and arc
endowed with the slender-waisted elegance of a greyhound."
MALE COMPETITION Their society is organized in the standard mammalian pattern. \
TO FEMALES A band of females accompanied (usually) by a single male.
The females are related, remain in the same territory and
society all their lives, and recruit new band members from
among their daughters. The males compete among each other
ANY POWERFUL TOOL CAN BREAK DOWN OR GO OUT OF CON- for residency rights; the right to live with the females. Sons
trol from time to time, and sometimes females find themselves are driven away from the troop when they mature and will
being drawn to their cost into the fierce dynamics of male only rejoin troop life when and if they succeed in usurping a
competition. In some cases their physical survival might be resident male of some other troop.
threatened, as in the case of the observations Merle Jacobs The actual displacement is accomplished by a group of
made on dragonflies (Plathemis lydia): males who first chase the former resident away and then
In many cases the female is chased by other males or is seized quarrel among themselves to see who gets to stay. Even males
while ovipositing [egg-laying] . . . . Many males may be in- securely in residence in one troop of females will reconnoiter
volved in this process at one site leading to a melee in which the situation in neighboring troops and attempt to take them
they dash at one another swiftly. . . . In these cases the female, over and succeed in being a resident in two troops at once.
being unable to oviposit, may fly from the pond followed by The result of all this restlessness is that sexual change is a way
many males, some of which have come from adjacent areas. of life among the langurs; males come and males go. On
Kingbirds may fly into these flocks and catch males, or, more average, a newly resident male can expect about twenty-seven
frequently, the slower-flying females. months of tenure before another male defeats and ejects him,
When two males simultaneously begin seizure of a female just as he had ejected his predecessor. (This is about the same
she may be injured and drop into the water. Wolf spiders often length of time as it takes for one of his daughters to reach
catch such females. sexual maturity. A troop that changes its male every two and
Or the costs may be inflicted on the females' offspring. A a half years thus prevents inbreeding.)
famous example of this are the pups that are crushed by ele- In 1963 some Japanese primatologists were tracking langurs
phant seal bulls as they plow back and forth across the shoreline through the teak forests of southern India when they saw a
attacking and fleeing from each other. There is no reason why a band of seven langur males drive out the "leader" of a troop.
130 / WHY MALES EXIST The Cost of Male Competition to Females / 131
One male among the seven remained with the females . Within old female named Sol, had no infants. Although Mug was able
days all six infants were bitten to death by the new male. This to return to his troop for extended visits, whenever Shifty left
I report seriously conflicted with the prevailing belief that a

healthy, "natural" society is one that harmoniously enlists the
energies of all its members and functions for the good of all.
The observation by Sugiyama was interpreted as a symptom
of some pathology or other, no doubt induced by the malign
Bazaar troop on reconnaissance to Hillside troop, Mug fled. On
at least eight occasions, Mug left the troop abruptly just as the
more dominant Shifty arrived, or else the "interloper" was
actually chased by Shifty. Typically, Shifty's visits to Hillside
troop were brief, but if one of the Hillside females was in estrus
he might remain for as long as eight hours before returning to
influence of human civilization. Bazaar troop.
Hrdy spent two to three months each year, from 1971 to During the periods Mug was able to spend with his former
1975, watching five langur troops that lived on Mount Abu in harem he made repeated attacks on the infants that had been
Rajasthani. Among these troops were two she called Hillside, born since his loss of control. On at least nine occasions in 1972,
whose resident male was named Mug, and a neighboring troop Mug actually assaulted the infants he was stalking. Each time
called Bazaar (because its inhabitants foraged in the local one or both childless females intervened to thwart his attack.
bazaar). Despite their heroic intervention, on three occasions the infant
was wounded. During this same period, other animals in the
In June 1971 the Hillside troop contained one adult male, troop were never wounded by the male. When the same male,
seven adult females, six infants, and one juvenile male. In Mug, had been present in the troop in 1971, he had not attacked
August of that year, Mug was replaced by a new male, Shifty. infants. Similarly, during Shifty's visits to the Hi11side troop in
. . . At the time of the takeover, one adult female and all 1971, his demeanor toward infants was aloof but never hostile.
six infants came into estrus and solicited the new male. [Copu- Whereas Hi11side mothers were very restrictive with their in-
lations are initiated by the females.] Local inhabitants witnessed fants when Mug was present, gathering them up and moving
the kiIIing of two infants by an adult male. Each kiIIing took away whenever he approached, these same mothers were quite
place at a site well within the range of the Hillside troop; in casual around Shifty. Infants could be seen clambering about
fact, one occurred at a location used extensively by that group. and playing within inches of Shifty without their mothers taking
It seemed highly probable that the missing infants had been notice.
ki11ed, and that the usurping male Shifty was the culprit. In 1973 Mug was joined by a band of five males. Nevertheless,
On my return to Abu in June 1972, I was surprised to find the double usurper Shifty could still chase out all six males when-
that the same male, Shifty, had now transferred to the neigh- ever he visited the Hi11side troop. A daughter born to Pawless
boring Bazaar troop. In 1971 , Bazaar troop had contained three during the period when both Shifty and Mug were vying for
adult males, ten subadult and adult females, five infants, and Control of Hillside troop was assaulted on several occasions by
four juveniles. Three of these infants were now missing. The the five newer invaders; the infant eventually disappeared . . . •
kiIIing of one had been observed by a local amateur ornitholo- By 1974 Mug was once again in sale possession of the Hi1I-
gist who lived beside the bazaar. The three Bazaar troop males side troop and holding his own against Shifty. When the Hillside
remained in the vicinity of their former troop; the second-ranking and Bazaar troops met, Mug remained with his harem. On several
of these bore a deep wound in his right shoulder. occasions, the newly staunch Mug confronted Shifty and in one
During 1972, Mug took advantage of Shifty's absence to instance grappled with him briefly before retreating behind
return to his former troop. At this time Hi11side troop consisted females in the Hillside troop. Mug resolutely chased away mem-
of the same six adult females and their four new infants. Two bers of a male band who attempted to enter his troop. . . .
females, an older, one-armed female called Pawless and a very When I returned to Abu in March of 1975 Shifty was no
longer with the Bazaar troop. In his place was Mug. . . . fifteen takeovers in all. At least nine coincided with attacks on
Mug's former position in the Hillside troop was filled by a or with the disappearance of unweaned infants; thirty-nine
young adult male called Righty Ear. Righty (with a missing infants are known to have vanished during takeovers. These
half-moon out of his right ear) was one of the five males Who
attacks only occur when the m ales enter the troop from out-
had joined Mug in the Hillside troop two years previously.
Since that time, Righty had passed in and out of the troop's side, generally for the first time, and in any event, as in the
range, traveling with other males but not (so far as I knew) case of Mug's first being ejected by and then replacing Shifty,
attempting to enter the troop. Righty's "waiting game" ap- after enough time has been spent away from the troop for
parently paid off in March, when he came into sale possession infants sired by another male to be born.
of the Hillside troop. But, as in the case of his predecessors, The key to this story is an adaptation langur females have
Hillside troop was only a stepping stone: In April 1975, Righty evolved to the loss of their infants (perhaps originally through
replaced Mug as the leader of Bazaar troop. attacks by leopards) . Ordinarily they have a single birth every
The first indication I had of Righty's arrival in Bazaar troop two years. But if they lose an unweaned infant the females
was a report from local inhabitants that an adult male langur immediately return to estrus and become receptive again.
had killed an infant. On the following day when I investigated Seventy percent of the females in Hrdy's sample who lost their
this report . . . an elderly langur mother still carried about the
infants gave birth again within six to eight months. Thus a
mauled corpse of her infant; by the following day she had aban-
male that kills the infants sired by his predecessor substantially
doned it. Righty subsequently made more than fifty different
assaults on mothers carrying infants. Nevertheless, only one advances the time at which females in his troop will begin
other infant disappeared. Five infants in the Bazaar troop re- bearing his offspring. Infanticide gives him a competitive ad-
mained unharmed when my observations ended on June 20. vantage over other, more tolerant males. To put it another way,
After Righty switched from Hillside to Bazaar troop, there a gene disposing a male toward infanticide would spread
followed some nine or more weeks during which the Hillside rapidly in a mating system like the langurs'. Further, the more \ .
females had no resident male except for brief visits from Righty. intense male competition is, and the higher the rate of turn-
Whenever the two troops met at their common border, Hillside overs, the more important such a strategy will be. Infanticide
females sought out Righty Ear and lingered beside him. These on this pattern has been found in lions and in every major
females were fiercely rebuffed by resident females in the Bazaar group of primates.
troop. Hostility of Bazaar troop females toward "trespassers" Male-male competition can work against the interests of
from Righty's previous harem prevented a merger of the two.
females in other ways. Certain mating interactions in some \
The troops were still separate . . . in October 1975, but the
species (the orangutang; some ducks, such as the mallard and
vacuum in Hillside troop had been filled by a new male, chris-
tened Slash-neck for the deep gash in his neck. 7• the green-winged teal) look remarkably like rape, though rape
seems strikingly rare in the animal kingdom as a whole. There
The sad story of the Hillside troop is obviously exceptional; are some birds in which the males are monogamous only so
otherwise there would be no langurs (during this period infant long as opportunity, in the form of other females, does not
mortality at Hillside reached 83 percent) . Another troop in present itself, at which point they will spread their parental
the area, presumably more normal, retained the same male energies over two or three broods. This is presumably good
from 1971 to 1974. But while the example is extreme, the for them but places an added burden on the females, or so
phenomenon seems to be a general one. one must assume. Theoretically, male-male competition would
Hrdy cites data gathered from three different locations- select males that speed through a series of copulations fastest,
even if that involves misleading, deluding, and outright lying agreeing that the services that males provide could be met by
to the females involved. a ratio of one son to every ten daughters. No doubt, continuing
Clear-cut cases of male lying are very hard to find , perhaps with this fantasy, all the females would agree that the idea had '\
because the females are too smart for them. Male deception great appeal, but whose son would be selected? Obviously
has been invoked to explain the evolution of empty "nuptial every male in this "reformed" system would father ten times
gifts" among a group of insects called the balloon flies. These the number of offspring as each daughter would mother. Un-
are flies that have been found to court females by offering them less the females imposed a convention on themselves, rein-
little silk balloons. A leading authority on these flies, Edward forced by policing and sanctioning mechanisms, cheating by
Kessel, believes that the practise took its first evolutionary step making sons would be automatically selected. (Here we see
in a species in which "the male avoids any cannibalistic atten- the same "anarchistic bent" that prevents predators from
tion on the part of the female by carrying with him, ready for establishing quotas or males from organizing themselves into
presentation at the moment they embrace, a wedding present a common front.) / L'M J~
in the form of a juicy insect." These males then evolved the So far as is known all females that live in fully interbreeding--r- --
habit of using silken threads to quiet the captured insects. Next populations divide their energies equally, on average, between
the silk threads became more elaborate and began to share, the production of sons and daughters. Some parasites do not
with the still relatively large prey, the function of stimulating live in interbreeding popUlations; brothers fertilize sisters, and
and attracting the females. The balloon appears in this stage. sons fertilize daughters. In these cases the mother can consti-
They are composed of beadlike chains of tiny bubbles, wound tute herself as a government of one and does indeed lay just
spirally into thin-walled, white or transparent, iridescent one male to a brood of daughters. The social insects do put less
spheres that look like tiny soap bubbles. As the bubbles be- effort into making males than females , but in these species the
came more attractive, the balloon took on a decorative role male role as a genetic emissary of the nest is reduced. If one
and eventually the prey vanished entirely. Finally, in Kessel's corrects for this by looking at the ratios of energy invested in
last stage, the male spins his balloon without incorporating any each sex in proportion to its genetic significance, one finds, as
elements from prey insects at all. Trivers and Hare did, that these ratios still equal each other.
The theory behind this is that the females were so taken This homeostatic equilibrium does have a loophole, since
with the little silk baubles that they no longer demanded real it does not apply strictly to the production of equal numbers
food. Assuming that the males are able to reuse the balloons but to the mother's energies, to how she trades off investment
over and over again, then spinning one balloon once rather in each sex. Sons and daughters should each take about the
\ than catching a number of insects might yield a competitive same size bite out of her reproductive life. If sons take more
advantage. Still, deep down inside I cling to my prejudice that energy to make, perhaps because they are bigger, then fewer
the balloon-fly females are not being fooled, and that the last of them will be made.
word on these species has yet to be written. Suppose that something in the environment kills males more
Is there anything females can do to control the ravages that often than females . The sex ratio among adults would be un-
male-male competition can wreak upon them? One possibility equal, and those males that survived would indeed father many
is that they might just make fewer males. Theoretically this more offspring than the average female. But mothers would
might be managed. One can imagine a grand council of all still not be selected to make more sons, because so much would
the langur, or dragonfly, females from an area meeting and have to be taken away from making daughters to be confident
136 I WHY MALES EXIST The Cost of Male Competition to Females I 137
of raising just one more reproductively effective, surviving son eaters. It is easy to see why, in this case, males cannot just
that it would just not be worth it. The bottom line for the simply stop killing infants. By the time a tolerant male had
langur females is that if leopards regulate the numbers of come to the end of his tenure as resident (twenty-seven months
males, then the pressures of male-male competition will slacken on average), most of the infants which he had patiently waited
off and infanticide with them. There can be no selection for to father would not yet even be weaned, and would be
females to make more males if some objective, implacable, un- murdered by the next, presumably infanticidal, male.
manipulatable force is doing the regulating. But the langur Hrdy did see a number of signs of female counter-strategies.
females cannot do it themselves, because it is their own sons When a new male takes over, certain females of the troop,
that are the problem. especially the old and childless, may combine forces to resist
In fact, in certain circumstances, a mother might actually his attacks on the troop's infants. Pregnant females sometimes
be selected to allow or even promote the exploitation of her display solicitation signals to a new male; since they could not
daughters as an instrument in male-male competition. This possibly be ovulating at the time, this might be an attempt to
would happen if the benefits that flowed to her sons were large confuse the male about the paternity of the infant-to-be. Once
enough to outweigh the costs levied against her daughters; such a female in a recently usurped troop, who had been traveling
a female might end up with a net advantage in grandchildren apart from the new troop (perhaps to avoid the new male's
over one that did not participate in that behavioral system. assaults), was seen leaving her partially weaned infant in the
For instance, the langur males that first evolved an inheritable company of another mother. She then returned to the main
tendency toward infanticide might well have had an extra- body of the troop alone. In three instances females with un-
ordinary reproductive success, if langur society was anything weaned infants left recently usurped troops to spend time in
like it is today, organized by residents, with male invasions and the vicinity of males that Hrdy believes were the fathers of
turnovers. If so, females that passed on to their sons a tendency their offspring. When a strange male or group of males invade
toward tolerance would have found themselves selected against. a troop, the females fight with the current resident against the
But this could only work over the short run, while the invaders. Usually these struggles involve cuffing and chasing
genetic context for infanticide was spreading and there were and noise-making, but sometimes they go beyond that. In
"tolerant" males to compete with. Eventually all the males 1882 a Victorian naturalist watched an especially bloody
would be infanticidal. The average reproductive success of encounter:
males carrying the genes predisposing toward infanticide
would have returned to that which males had had before the . . . Two opposing troops [were] engaged in demonstrations
behavior evolved at all. There would be no one left to compete of an unfriendly character. Two males of one troop [apparently
these were the invading males] ... and one of another-a
with (on this issue). What would be left would be all those-
splendid-looking fellow of stalwart proportions-were walking
slaughtered infants; all that wasted female energy. At this around and displaying their teeth. . . . It was some time-at
point, if and when a counter-infanticidal strategy emerges, it least a quarter of an hour-before actual hostilities took place,
1 could spread and succeed on its ability to 'bring to maturity when, having got within striking distance, the two monkeys
those infants that would have been killed. made a rush at their adversary. I saw their arms and teeth going
At least that is the theory; unfortunately for the theory it viciously, and then the throat of one of the aggressors was ripped
looks as though infanticide is both universal and very old in right open and he lay dying.
this whole subfamily of monkeys, the colobines, or leaf- He had done some damage however, before going under, hav-
138 I WHY MALES EXIST
ing wounded his opponent in the shoulder... . I fancy the tide
of victory would have been in [the other invader's favor) had
the odds against him not been reinforced by the advance of two
females. . . . Each fiung herself upon him, and though he
fought his enemies gallantly, one of the females succeeded in
CHAPTER
XIII
seizing him in the most sacred portion of his person, and de-
priving him of his most essential appendages. This stayed all
power of defense, and the poor fellow hurried to the shelter of
a tree where leaning against the trunk, he moaned occasionally,
hung his head, and gave every sign that his course was nearly
run. . • . Before the morning he was dead.'" MALES WITH AN EDGE
As diverse as all these strategies are, they are not effective.
The infants still die, and, as we saw in the case of the Hillside
troop, sometimes at such great rates as virtually to ensure the A MALE READING ALL THIS MIGHT WONDER IF THERE IS ANY
extinction of a troop. It is something of a mystery why the end to the demands that females can make upon males. Do '1
langurs have not succeeded in breaking out of the box into any members of the gender ever manage to climb out of their
which these excesses of male-male competition have led them. inferior position? Do females always have everything their
Hrdy mentions two possible counter-strategies. The first is that own way? Obviously to the degree that female demands drive
the females could organize. They could refuse to copulate with down the number of competing males, either by killing them \
an infanticidal male, or not advance their ovulation cycle after through exhaustion or by forcing them to spend a lot of time
one of their infants died, or form a unified force that would over each female, then females will have fewer males to play
punish infanticidal attempts severely. Or they might grow off against each other and will have to temper their levies
larger than the male; this would put single females in a position against male energy. So there are some limits built into the
to punish infanticidal males (presently langur males weigh system. Since male competition has, in some species, made
about eighteen kilograms; the average female weight is twelve males larger than females, males sometimes have a competi-
kilograms) . It has been proposed that the reason why the tive advantage in nonmating interactions, like squabbling over
hyena female is larger than and dominant over the male is for food. (Though in actual practise "dominance" can shift back
just this reason, to prevent males from threatening her cubs. and forth, depending on the issue, the reproductive state of
But for whatever reason or reasons the langur females have the female, and other factors besides size or weight.)
not taken either route. The point of this melancholy tale is One exception to the picture of males conforming to female
that systems of male-male competition can arise that end by needs is the lek displays, in which males seem to organize
leaving both sexes trapped in a behavior that is to the advan- themselves and pull the females toward them, rather than the
tage of neither. other way around. Lek displays have been interpreted here as
existing because they allow females to shop for mates among
a larger number of candidates and pick the single best-
however "best" might be defined-of all the males in the
area.
140 / WHY MALES EXIST Males with an Edge / 141
Thus the real actors in the system are not all the males The examples of male incitement given earlier in chapter
and all the females, but a tiny handful of highly attractive eleven may have seemed like a tyrannical assertion of au-
males-a large population of peripheral males whose unwill- thority. Still, looked at from the point of view of the dominant
ing role is to provide a background against which the winners male, male incitement is simply a request by the female that
can identify themselves to the females. Despite there being he step forward, brush aside some pathetic competition, and
dozens or hundreds of physical males on the lek, there are mate with her. What could be more convenient for him than
usually only one, or two, or three reproducing males. These that? Without her call he would have to keep all the males in
reproducing males have a much more powerful leverage po- the area continuously suppressed; incitement serves his in-
sition vis-a-vis the females; in effect they get the females to terests by making it possible for him to arrange his time more
inconvenience themselves as much as the males, in that both efficiently. If female lizards (Anolis carolinensis) are exposed
sexes now have to travel to the lek. (If there were only one to the sight of male aggression, of males fighting over domi-
acceptable male in the population he wouldn't have to go any- nance position, their ovaries either will not grow or will shrink.
where; all the females would have to find and pursue him.) They thus postpone their mating to conform to the dominant's
Both the winning males and the females exploit the peripheral schedule, until such time as he has vanquished the competi-
males, who carry the burden of advertising the quality of tion. They are dependent on the dominant for something,
the central males to the females, but get nothing out of it perhaps a quiet, trouble-free mating, or his genes, or both,
themselves except perhaps a learning experience. The greater and that dependence has forced them to pay attention to his
advantage of central males can be seen in other ways than that problems. Female baboons have an estrus patch that flames
they get the females to come to them. A study of lek displays out brightly when they are at the peak of their receptivity.
in the greater prairie chicken (Tympanllcilus cupido pinnatus) Again, this is a great convenience for the dominant male,
showed that central males spend less time courting females who can monitor the cycles without going to any more trou-
than do the peripheral males, and yet still get by far the pre- ble than you or I might go to in glancing at a wristwatch.
ponderance of copulations." If for some reason a preferred There are a number of species in which females are de-
male is available only for a short period, then females might pendent upon a resource which is controlled by males. The
be selected to conform to his schedule rather than the one males that possess the richer resources usually get more fe-
most convenient for them. Cox and Le Boeuf note that: males, which is an example of females indirectly accommo-
dating themselves to males. Good examples of this are found
Since there is a limit to how many females an alpha male can in marsh birds that can live either monogamously or biga-
inseminate . . . it would be advantageous for a female to mate mously; whether a male lives with one female or two depends
with him early, when he is fresh and before his fertility or sexual
on the quality of his territory.
interest starts to decline. . . . We know that females who ar-
rive early in the season form the center of the harem (and are The African, or black-headed village weaverbirds (Ploceus
therefore) more likely to copulate with the alpha male than cucullatus) have the potential for illustrating these points in
females on the periphery, because the alpha male takes up a a much more subtle and interesting way. The weavers belong
central position among the females. . . . CentcallY located fe- to a group of twenty-seven species, all of which live in Africa,
males are aggressive to females on the edge and keep them from that build (weave) tightly woven, quasi-spherical, enclosed
entering the center of the harem, and early-arriving females may nests, usually with a downward-pointing entry hole or tube.
prevent late-arriving females from joining the harem. The nests hang from the outermost twigs of trees, often over
water. The point of these enclosed, hanging nests is thought feathers erected often to their fullest extent. The wings mayor
to be protection from predators, including hawks, kites, and may not be quivered, depending on the intensity of the dispute,
eagles from above, genets, wild cats, mongooses, and jackals and the tail likewise may be fanned out only at higher intensity
from below, and a number of tree-climbing pythons. The vil- levels. As one male sings, the head is bowed, the beak is pointed
lage weaver gets the first part of its name from a taste for downward . . . and the black head with blazing red eyes con-
building near and in human settlements, and probably this is trasts conspicuously with the yellow on body and wings. Fre-
also, in part, an antipredator strategy. quently the birds sing alternately, each uttering some short pre-
In 1967 two California zoologists, Nicholas and Elsie Col. liminary notes terminating in a longer buzz. The song often
seems to inhibit attack from the opponent for the moment, the
lias, spent seven weeks in the Senegal River Valley watching
birds appear to be listening one to the other, and may alternately
some colonies of weavers nesting in trees tbat overhung irri. advance and retreat, sometimes swaying the head slowly to one
gation canals and streams. (The countryside is often arid and side as if with the intention to turn away and move off. . . •
the weaver is dependent on these streams for drinking, bath.
ing, the vegetation used to build their nests, and the insect life After these intricate exchanges are complete the males
they feed their nestlings. Also, building directly over the water begin, each in his own territory, to build the shells of breeding
may be an antipredator defense.) The breeding season runs nests. The shells are woven from long (twelve inches to
throughout the last two months of the three-month rainy sea· eighteen inches) strips of palm leaves, sedge, and grass. They
son, which runs from July through September. One sign that are not crude affairs; for example, they have a double roof,
breeding activities are about to commence is that the males perhaps, the Colliases speculate, as insulation against the sun
change their plumage from the camouflage green-brown, with and rain. "We have seen no instance in nature where the fe-
a yellow throat, to a stark yellow and black. Their bills change male ever helped the male to weave the outer shell of the
from gray or ivory to black ; their heads from olive-green to nest," the Colliases write. "However, we have had one ab-
black. Black patches appear on each side of their beak. The normal female in our aviaries who wove several nests by
nape becomes a rich chestnut. The males then partition the h~rself and even laid eggs in some of these after copulating
branches of the breeding tree or trees among themselves with With the male who held the adjacent territory." A male may
a range of aggressive interactions that range from simple and bUild a nest in a single day. The "average" male built four
quiet exchanges to vicious head-pecking battles. The Colliases nests in all. The males seem not to call continuously for fe-
carefully distinguish among six different levels of aggressive- males but wait for them to arrive. When one does:
ness, but it is clear from their detailed descriptions that they . • . he goes to his most recently built, greenest nest and
could just as easily have built a case for twenty. As an exam- hangs upside down fluttering directly beneath the nest, showing
ple, here is their description of level four: t~e entrance to the female. . . . The inverted male clings with
hiS feet to the inner lip of the entrance, flapping his widely
Song and full plumage displays are given during formalized opened wings and repeatedly uttering characteristic notes which
border disputes or between two males seriously contesting for we verbalized as look-see! look-see! . . . At the same time the
dominance. Sometimes a male holds a piece of nest material in male rocks or swings from side to side, all the while keeping his
his beak when defending his territory. . . . Sometimes one of feet at the same place on the nest. . . .
the contesting males wipes his beak against a twig as if removing The beating of the male's wings is made more conspicuous by
some distasteful object. The two males crouch forward facing the bright-yellow underwing coverts, and the spread wings re-
each other with the neck drawn in and the head and body veal the yellow color on most of the feather shafts. . . . The
whole effect of the continuous movement and shifting brightness desirable to males, and all males uniformly uninteresting to
pattern of the wings during the nest invitation ceremony is females. But I have only mentioned one side. At the same
reminiscent of a flashing yellow light. A whole colony of males time as the Colliases were noticing most females hemming
simultaneously displaying their nests to visiting females is a and hawing and delaying copulation, they were also noticing
conspicuous and spectacular sight. some females accepting a nest and copulating with a male
within a few minutes of arriving on the scene. They even saw
The female usually hesitates for some time in front of the one female fly right by a hesitating female and shoot into the
displaying male, who may fly back and forth between her nest herself. When a male is courting a female he sometimes
and his nest, singing constantly to her with a rich variety of drives off the other females in his territory. The reason he
songs. (The neighboring males also try to catch her atten- does this, the Colliases believe, is that resident females will
tion.) If the female leaves the territory the male may build sometimes interfere with the courtship of a new female. Once
some fresh nests; if a specific nest has been repeatedly rejected, they were watching a male displaying a nest to a visiting fe-
or begun to fade, it will be dismantled and a fresh one hung male that already had a female resident within. Suddenly the
in its place. If a female enters the nest she will poke and pull resident put out her head, grabbed the male by the feathers
at the materials for one to more than ten minutes, then may on the top of his head, and hung on for about twenty seconds
leave, return, and reinspect a nest several times before ac- while the male tried to free himself. Then she ducked back
cepting it, if she does. (The hanging display of the male might into her nest. The male flew off and did not display this nest
be interpreted as being, in part, a stress test of the nest. again for at least thirty minutes, after which time the Colliases
Weavers breed in the rainy season, and their nests, which stopped watching. Why should the female have interposed her
hang free, out in the open, can be violently tossed about by desires in this way? The point is that males sometimes "change
the strong winds and heavy rains.) If she accepts a nest the their mind" about which female they prefer, will pull an
male begins to look around for another female (the "average" already-resident female out of her nest, send her off, and dis-
male has two) and she lines it, often beginning with a thin play that nest to a second female! Presumably the female
foundation of leaf strips, then a layer of soft grass heads or that grabbed the male was (successfully) preventing any
feathers. Frequently a male sings to a new mate each time chance that "her" male's enthusiasms might be won over by
she enters the nest with a beakful of lining material. He is some other female for whom she would be evicted.
excluded from the nest; should he try to enter the female ut- These are the clues of a very different balance of power,
ters a loud "protest" call and the male "invariably" desists one in which a male or a class of males, has something to
and leaves. When pecked by one of his mates in his tree offer which a female finds useful enough so that she learns
territory he ordinarily yields to her and does not peck back, to grab it without delay when it is offered and fears competi-
though outside his territory, on the ground, he will shoulder tion for it from other females. There is nothing in the Col-
his way ahead of the females if any food is presented to them. Iiases' report that allows one to decide what that quality or
The Colliases report that in their aviaries, if a male has no resource is, but there are a number of possibilities. One is
nest in which to sleep, he does not oust a female from one nest location. Nests in the upper parts of trees were found
of the nests he built but sleeps in the open. to be less likely to be occupied by females than those hanging
All this seems a very straightforward picture of a rather directly over the water. The reason for this is not hard to
common system in which the females are all equally highly find. Pythons attack the weaver nests by crawling out over a
lower branch and raising their body up to the level of their then expand their body size by about 25 percent each time
target. If only a small percentage of the males are able to and rebuild their skeleton out of elements filtered from the
acquire territories on the most secure branches, females might sea water and recycled from their old shells. The new shell
compete among themselves for residency rights in those nests, does not harden enough to provide good protection for
and the males that controlled them would be presented with seventy-two hours, and usually, when crabs molt, they stay
a choice of mates. A second possibility is nest construction. buried in the sand for at least a day or two. Females mate
Perhaps a fraction of the weaver males are much more highly once, just after they have completed their last molt. Obvi-
skilled (maybe because they are older and more practised) ously a female that first cast her shell and then broadcast
at building nests. If this edge in workmanship has important receptivity pheromones while buried in this condition would
consequences, then females might compete to be the mate of risk being found by predators as well as males, while a female
an older male. The third possibility is good genes. If the early that hid effectively enough to escape from one might be missed
territorial battles define a small class of winners, then those by the other. The blue crab has responded to these exigencies
winners might have genetic qualities that make them highly by evolving a very elaborate system of courtship and mating
attractive as mates. What I would guess is that as males get behavior that will allow successful fertilizations to take place
older they get better in everything. They win more territorial even while the female is at her most vulnerable.
battles, their nests are more skillfully built and located, they A typical fertilization sequence might run like this: First
become more adroit at courtship, and more aware of the the female releases a pheromone. If a male is nearby and
dangers of the environment. The prediction is that evictions attracted he will approach the female and begin his display.
will be found to be conducted exclusively by older males, In this he raises his body as high as he can and walks around
because older weaver males might be in the position that is her on tiptoe, opening and extending his claws, and lifting
occupied by females in most species: they attract a surplus his flatter, rearward, swimming legs up over his body to form
of mates and so are free to indulge preferences. two waving, parenthesislike arcs. All these behaviors make
Another way in which a fraction of the male gender might the crab look much larger and more formidable than he really
find itself in a more favorable power relation to the females is (to a human, anyway). During his display the male snaps
than males usually enjoy might be as members of a "chrono- his body backward and kicks up flourishes of sand with his
logical elite". This might occur in species in which females legs. Sometimes the male will repeat this whole routine over
strongly prefer to be mated within a very short time, too and over, while the female rocks from side to side and waves
brief a period for males to be able to travel to more than one her bright red claw tips. Sooner or later one sex or the other
female (or even as many as one; the evolution of this system takes the initiative and the female ends up tucked beneath (\
requires that some females have to accept fertilizations out- the male. He then swims off, holding her under him, searching IJ
side the optimum period and suffer reduced reproductivity for eelgrass or some other hiding place. There is some evi-
thereby). One species in which this seems to have happened dence that the search for a suitable site can continue for as 0
is the Chesapeake Bay blue crab, Callinecles sapidus Rath- long as a week, though two days appears to be standard.
bun, the "beautiful tasty swimmer". When an old coffee can, or patch of grass is found, the male
Crabs, of course, have an external skeleton (the word stands over the female and makes a cage with his legs. The
"crustacean" comes from the same root as "crust"), which female undergoes her last molt, which might take two or
they cast off about twenty times over their life cycle. They three hours. William Warner, whose Beautiful Swimmers is a
natural-social-history of the Chesapeake crabs and the Chesa- months of growth the hatchlings have begun to look like
peake crabbers, describes the act of fertilization: crabs, though as yet they are only one-tenth of an inch wide.
When at last the female lies exhausted and glistening in her They begin to migrate up out of the ocean and southern Bay
new skin, he allows her some moments to rest and swallow the into the rivers and upper Bay. They overwinter in Virginia
water that is necessary to fill out her weakened stomach and waters, south of the Potomac, and resume moving up-Bay in
muscle tissues. This done, the male gently helps the female turn the following spring and summer, during which time they
herself about-she may well have gotten impossibly oriented in grow to adulthood and mate. The females then return to the
the final throes of ecdysis (molting)-until she is on her back lower Bay and ocean to spawn; the males remain in the
face-to-face beneath him . . . . When the female crab is ready, brackish, up-Bay waters and continue to seek females.
she opens her newly shaped abdomen to expose two genital Blue-crab males devote a considerable amount of time to
pores. Into these the male inserts two appendages. . . . When their mates, four days or more, during which they are out
all is in place, the female so extends her abdomen that it folds of the mating pool. Especially when the mating season is just
around and over the male's back, thus . . . preventing any risk beginning, in May, acceptable males will not be as ubiquitous
of coitus interruptus. They remain thus for from five to twelve
hours. as males usually are. Yet a May fertilization seems to be the
optimum for females, giving them time to reach the ocean that
For another two days or so, until her shell hardens, the summer and perhaps even generate two spawn. Females that
female is cradle-carried by the male. "To think properly about mate in the summer have to overwinter in the Bay and then
the blue crab," Warner writes, "it is first necessary to assume spawn the following spring, nine months after having been
that the species can and will perform anything in its life cycle fertilized. Aside from the added mortality this implies, there
at any time, dead of winter excepted." That warning in mind, is some evidence that such females do not have the option of
one can say that in terms of crude averages, mating begins spawning twice.
in early May, reaches a peak in late August and early Sep- Females therefore need males most when the sex ratio is at
tember, and continues into October. It takes place high in its lowest, and they respond by seeking males out actively.
the bay, a long distance from the ocean, where the female A branch of the crabbing industry, called "Jimmy potting,"
spawns. Once a female has been fertilized she travels down has sprung up to exploit this rare business of male hunting.
to the Atlantic. Females that have been fertilized early in the Male crabs, called Jimmies, are placed in a pot and sub-
year can make it in one trip; other females overwinter part- merged, or tethered, on a string. Then, when females that
way down and finish their journey in the subsequent spring. have been attracted by the males appear, they are caught.
A spongy egg case containing from seven hundred thousand Warner quotes one crabber: " . .. I remember one Jimmy
to over two billion eggs is constructed over the two months I had on the line, now he caught seven wives just as fast as
after fertilization. When the female reaches the ocean she he could get them. I just stayed there taking them. Then
passes her eggs from her ovaries past the reservoirs where she all of a sudden he wouldn't catch any more. I couldn't blame
keeps and maintains the sperm. The mass of fertilized eggs is him none. . . ." Jimmy potting can only be practised at the
attached to hairs on the outside of her abdomen, where very beginning of the mating season, in May and early June.
she carries them until they hatch. If conditions are good the Thereafter, one assumes, enough mated females have left the
female can generate and fertilize a second batch. After two population so that males tend to be on hand when the time
for the final molt arrives; the females do not need to look
for them, or depart from their foraging routines to follow a
male scent.
Blue-crab behavior is extremely flexible. Sometimes the
male attracts the female; sometimes the other way around.
CHAPTER
XIV
Generally the male goes through an elaborate courtship dis-
play, mentioned above, in which he seems to be demonstrating
his capacities for dealing with the responsibilities he is about
to undertake-showing his height, and thus what kind of cage
he can make, his breadth of reach, and his strength-but the
female also (sometimes) waves her brightly colored red claw
MALE LEVERAGE
tips, an action that can plausibly be thought as intended to AND EQUAliTY
stimulate the male. (Only the female thus "paints her finger-
nails," to use the Bay expression.) At other times the female
simply scoots under the male with hardly any preliminaries
at all. Sometimes females are seen rejecting males, or mating THE USUAL RELATIONSHIP BETWEEN THE SEXES CAN BE
with more than one. One possible explanation of this vari- reversed for a number of reasons. First, if there are so few
ability is that the blue crab is adapted to a breeding season males that females cannot afford to wait for more than one
in which the value of males begins high and then steadily candidate to appear, then females will lose their usual lever-
sinks all summer, and that crabs have evolved ways of as- age. When Merle Jacobs, as part of his study on dragonflies,
sessing this swinging balance of desirability and altering their removed all but a few males from his study pond, he found
mating behavior accordingly. that the dragonfly females took to pursuing and pouncing on
Over the last few pages of this chapter different means have the remaining males. The males copulated at abnormally high
been reviewed as to how a fraction of the male population frequencies and finally left the pond altogether, presumably
might climb out of the inferior position in which most males having found themselves in the unusual position of running
find themselves vis-a-vis females. All the systems presented out of sperm and energy before running out of mates. Obvi-
left the majority of the males, over a majority of the breeding ously when courtship (or just the fact of being male) becomes
season, as the "go-fer" of the mating interaction. The only so taxing that it removes males from the mating population,
way in which the majority of males in a species can have an then females will have fewer males to playoff against each
equal relationship with their females is by attacking the root ollier and will have to stop making demands on llieir time
of the asymmetry between the two-the difference in repro- and energy.
ductive tempi. In the next chapter we will look at some species Second, females might very strongly prefer, as mates, just
that have managed to reduce this distinction between the a fraction of llie available males. H a good male is hard to
genders. find, then assuming that the female cannot wait forever, she
will have to go and find one herself. A male might possess an
exceptionally attractive resource of some kind, one that can-
not support all llie females that would like to gain access to
152 / WHY MALES EXIST Male Leverage and Equality / 153
it. A propertied male of this sort might even be selected to given the rigors of travel, it may be impossible for a male to
pick and choose from among the females contending for fertilize more than one female in a season. In these cases he
access to his territory. The issue of females' being attractive is more likely to live in some kind of association with a single
or not would become important. This would be a 180 degree female and wait for her to become ready to breed over a
reversal of the usual mating relationship. number of seasons. For example, there are about two dozen
A third class is made up of cases in which males do not species of small African antelopes, mostly forest-dwellers,
compete for more than one female. At an extreme this might
be because copulation is fatal or severely debilitating to the
male. Sexual cannibalism in mantids and spiders is one exam-
that live monogamously in this way. Small antelopes (the
smallest is only a foot tall at the shoulder) virtually never
gather into herds. For one thing, their small size commits
(
ple. A second example, surely very unusual, has been found them to easily exhausted high-quality food items. (A small
in an Australian marsupial shrew (Antichinus stuarti); copu- warm-blooded animal loses heat faster than a large one, which
lation unleashes in the male a fatal surge of corticosteroids. is why hummingbirds and shrews have to eat continually. A
The males of a group of neotropical frogs (genus Atelopus) smaller antelope is therefore more likely to specialize on just
fasten onto the backs of females weeks and even months be- the high-protein parts of plants.) Thus competition from
! fore those females are ready to lay their eggs. For some rea- other members of their herd would be especially burdensome;
son the female does not scrape the "piggy-backing" male off and their main defense is an ability to forage inconspicuously,
and carries him until she needs her eggs fertilized; during all which is hard to do in a group.
this time the male does not eat and grows progressively more Both these life strategies require that the antelope have
emaciated. While little is known about this group of species, .
it seems unlikely that these males will be able to mate with
more than one female in a season-maybe in their life.
an intimate knowledge of every nook, cranny, bud, and twig
in his/ her territory. Members of these species thus tend to
live solitary and rooted lives. The males and females may
\
Examples like these might be considered to be the simplest live as pairs or they may live in adjacent territories and asso-
form of monogamy. Usually what we mean by that word ciate only at mating time. In either case the costs of travel
involves a period of association between the genders, often, in these species are so high that males end up just mating
though not always, extending over more than one breed- with a single female.
ing cycle. The firmest of these associations are obviously Other circumstances that can force a monogamous society
those built on the model of the angler male; I know of no include highly unpredictable mating opportunities. There are
f other in which the male is fed, like a fetus, via the female'S
blood stream. There are quite a number of parasitical and
two groups of parasitic birds that lay eggs in other birds'
nests. In one group the males travel around competing for
other filter-feeding invertebrates, such as some barnacles, that females with distinct, conspicuous displays. In the second,
have adopted a "dwarf-male" system in which the sperm which includes the more familiar cuckoos and cowbirds, the
donor is either physically attached or lives in very close asso- two genders look alike and live monogamously. The differ-
ciation with a much larger female. Monogamy often seems ence seems to be that the monogamous parasites specialize
associated with female dispersion and a lack of mobility. If on the nests of a single species, while the promiscuous birds
\ the females of a species do not herd or group themselves in (Molothrus ater, M. bonariensis) can lay their eggs in the
any way, if they do not gather to compare mates at a lek, nests of many host species. These generalist parasites lay
if they are not committed to a communal breeding site, then, more eggs (though perhaps their eggs are tossed out more
often by the host parents, since their eggs are not such skillful then excavate the soil beneath or around the body, .. chew
copies of the hosts' as are the specialists'). Any nest parasite, and manipulate the putrefying mass until it is roughly spherical
whether generalist or specialist, has to lay her eggs expedi- in shape . . . then seal off the burrow from below, entombing
tiously, during the period when the brooding bird(s) has left themselves with the rotting ball.
the nest to forage. If specialist parasites have fewer of these
opportunities, which are not especially predictable, then they When the larvae hatch they sit in a crater formed by the
have to capitalize on them all the faster. Under these circum- female on the food ball. For much of their development they
stances it may well be better for a male to attach himself are partly dependent on regurgitated food; this is usually
permanently to a single female rather than risk visiting a supplied by the female, though in two of the six European
number of females, but never arriving at quite the right species of Necrophorus the male helps feed the young to a
moment. The more promiscuous generalists, by this theory, limited degree. (Two University of New Hampshire ecologists,
have enough targets so that the females can take the time to Lorus and Margery Milne, studying American species of this
be courted.· insect, have noticed that in some cases, after the food has been
The fourth class of "powerful" males are those in which buried, the male copulates and then buzzes off, leaving the
members of that gender provide some kind of parental care. female to minister to the young herself. But by then the most
This could include feeding and! or guarding the female; important piece of work, locating and secreting the food, has
brooding, feeding, guarding, or tutoring the young; maintain- been accomplished.)
ing the site, or guarding the territory. All these forms are rare There are a few other examples of paternal care among
except in birds. Male parenting is virtually unknown among the invertebrates. Some male crabs protect the female during
the insects--one-third of all animal species. One of the very her molt. Male fiddler crabs of several species dig burrows
few known exceptions occurs among the burying beetles, into which females enter to deposit their eggs. I have seen
Necrophorus. E. O. Wilson gives a very succinct description only one reference to male parenting among worms; and that
of their habits in Sociobiology: was Neanthes caudata, a marine worm in which the male
incubates the eggsY'
In May the overwintered adults begin to search for the dead Paternal care is somewhat more common among the fish,
bodies of small vertebrates, such as birds, mice, and shrews. If
a male encounters a corpse, he takes the "calling" posture, lifting though surely found in fewer than 5 percent of all species.
the tip of his abdomen into the air and releasing a pheromone. Male seahorses and pipefish incubate eggs laid by the female
The substance appears to attract only females belonging to the in a special pouch. Paternal care is relatively widespread
same species. If more than a single pair find a corpse-and some- among the family Cichlidae, which are a very successful and
times as many as ten do--fighting ensues, male against male and species-rich group of fish. In some African species this care
female against female, until only a single pair is left. The winners might involve mouthbreeding, in which one or both parents
protect their eggs or young from predators by holding them
• Everything said in this section is based on the assumption that the adult
!
in their mouths. In other species, often .found in Latin Amer-
sex ratio is about equal, and it may be that in some of the species men·
tiaDed here-the mate-eating insects. the anglerfish, the piggy-backing frogs ica, the parents defend free-swimming broods, sometimes,
-the females afC in a vast minority, perhaps because they suffer differ- from just-laid-eggs to "graduation," over periods as long as
entially from the attentions of predators. In these cases the females that
survive will have so much leverage that the males will have to fight and three months.
qualify for the opportunity to mate even once. Kenneth McKaye, a biologist from Yale, has investigated
156 / WHY MALES EXIST Ma/e Leverage and Equality / 151
these fish and made some fabulous (and still very contro- foraging out on the sand-silt bottom of the lake. It only ap-
versial) discoveries. One of these was his report that of the proaches the lake's rock faces to look for holes in which to
nine cichlid species that live in Lake Jiloa, Nicaragua, at least breed. The holes it needs are also used as breeding holes by
four adopt foreign young-young of other cichlid parents, other fish species, including one in particular, Neetrop/us
sometimes even from different species--and integrate them nematopus, that competes for the same size holes, at the same
into their own brood. depths, and is a better fighter. These other species spend all
their lives living near the rocks, as does the predator, who
In two instances parents were speared and the unguarded
young were adopted by neighboring territorial pairs. We also eats them. It is especially fond of N. nematopus. The predator
saw territorial pairs take young of other pairs into their broods. has a hard time raising its young; all the prey species living
This occurred twice when pairs were engaged in a light with in the rocks attack their fry, for obvious reasons.
conspecilics. [Another] adoption occurred when one pair "kid- Given these facts, McKaye argues that it might be adap-
napped" some young of another pair. This happened when the tive for an altruist couple that has tried to breed but failed
(because the competition for breeding holes was too intense)
o
fry of both pairs were approximately three weeks old, but the
school of one pair was diffuse. When both parents faced away, to raise a big crop of predators. (Their help makes a big
the male of the second pair swam in and herded approximately difference to the success of the predator-parents, who do not
50 young out of the school and brought them back to his own bother the assisting couple in any way.) Then the altruist
school, which had about 150 young. couple swims back out to the middle of the lake while "their"
In water of two to three meters in depth three pairs of C. predators gobble up the competition that had been so bother-
citrinellum "communally" protected from predators a large
some. When they return they might indeed be subject to
school of four- to five-week-old fry. When danger threatened,
the young would split into three groups and follow the pairs attacks from the very fish they helped raise, but they would
back into their respective caves. When the danger passed they also have access to breeding sites, and that tradeoff, McKaye
emerged and mixed freely in the school. Individual fry were suggests, might be worth making.
observed switching parents. Paternal care in the amphibians and reptiles is also rare.
There is one family of neotropical frogs (the Dendrobatidae)
McKaye believes that if an adaptive explanation is appro- in which the eggs are laid on land and carried to water on
priate for these phenomena, it is probably that up to a point the back of an adult. Sometimes this adult is a male. Kent-
a parent can decrease the risk that one of his or her progeny wood Wells passes on this report of male parenting in the
will be taken by a predator by increasing the number of for- Panamanian poison-arrow frog (Dendrobates auratus) , so
eign fry around his or her offspring. (This point would be called because a toxin secreted by its skin was used by the
reached when the cloud of fry grew so large that either the Panamanian natives to tip their arrows.
parents' defensive abilities were overwhelmed or it attracted
\ a much higher rate of predator attacks.) I observed parental behavior performed by a captive male
He found something even stranger. Some couples were help- that mated with two females. After a clutch of seven eggs was
laid, the male sat on them three times in ninety-five minutes. In
ing their predators raise young! In eight cases he saw fish
each case, he sat on a wet rock in a shallow water dish for ten
helping raise other fish that, when grown, might eat them. to fifteen minutes before sitting on the eggs. Twice he remained
This might just be craziness, but, McKaye argues, not neces- on the eggs for twenty-five to thirty minutes. He did not sit
sarily so. The altruist, C. nicaraguense, spends most of its life passively, but moved in a circle and worked his legs in and out
158 I WHY MALES EXIST Male Leverage and Equality ! 159
of the jelly. The egg mass increased in size with this treatment, size is 2.2). Males defend feeding territories within which
suggesting that the male provided moisture from his skin. they find their insects. They defend these territories against
Males can care for more than one clutch at a time. I saw the both male and female jacanas, but since the females usually
captive male sitting on both a fresh clutch and a hatching clutch weigh some 75 percent more than males (and are dominant
in the same hour. [In another case a male left a spot where eggs over them), males usually succeed only in repelling invaders
had been laid. After two hours the male returned.] . . . He ap-
of their own gender. To drive out females they depend on
peared to search for the eggs in the leaves for twenty-seven
minutes, but was unable to find them, possibly because I had the resident female, who defends a superterritory that em-
disturbed the leaves. He moved up the slope and disappeared braces the ranges of two or more males. The females not only
into the litter five meters from the first site. I moved leaves aside help exclude invaders, but even keep the peace within their
and found him sitting on a clutch with three or four hatching "harem" by preventing incursions of one member onto the
tadpoles. territory of a second. "Such polyandrous females may copu-
. . . When eggs were nearly ready to hatch (after ten to late with a male a few minutes after driving him from his
thirteen days), the male sat on them, . . . with his back arched neighbor's territory," Donald Jenni, the foremost American
and his ankles pressed together, forming a sort of trough. Tho student of these birds, has noted. (A consolation copulation?)
male never [sat this way] on freshly laid eggs. The male scrapes together the nest, broods the eggs, and at-
tends and defends the young after the eggs hatch. The young
When the tadpoles hatched they wriggled up the "trough" can feed themselves, but are reluctant to do so except in the
and tried to attach themselves to the male's back. Some have presence of the father. Predation is in fact high; probably less
said that males of these species can carry more than one than 50 percent of the clutches are successful, and the males
tadpole, but Wells never saw more than one tadpole on a and females both spend a lot of time threatening, attacking,
male's back. The male then hops away, looking for a puddle, and distracting a whole zoo of avian, reptilian, and mam-
perhaps in a tree trunk, in which to leave the tadpole. malian egg and chick eaters.
Male parenting is practically the rule in birds-found in The females often mate with each member of their "harem"
probably 90 percent of the species making up the order. In a each day. Jenni says they display "an exceptional amount of
) few dozen bird species the pendulum has swung over on the
other side and the male provides most of the parental care.
overt sexual behavior." The precopulation ritual consists of
an initial display of female aggression, then male appease-
One theory has it that this happens when egg and! or clutch ment of the female, followed by female solicitation of a male
predation is especially intense. If the young are constantly mount (which the male refuses more often than not). Mating
being taken then it might be adaptive for both the male and is suspended while a male is incubating and until the chicks
the female for her to be ready to lay a new clutch at a mo- are six weeks old, whereupon it resumes-weeks before the
ment's notice, which would involve her being up and around male nests again. (The jacana breeds all year.) The female
and feeding instead of sitting on the nest. life-style seems clearly to be the more hazardous or exhaust-
One of the best-known cases of role reversal is the Ameri- ing, since females are displaced by other females twice as
can jacana (lacana spinosa), a tropical shorebird that lives often as males are by other males.
in freshwater swamps and marshes and feeds on insects. Fe-
males can have "harems" of males-stable pair bonds with
Paternal care among the mammals is not a great deal more t\
common than among the fish . The most famous single in-
more than one male simultaneously (the average "harem" stance is probably the male beaver, who helps build a dam, a
lodge, and accumulate a central food horde that will be having both parents in the nest means an increase in the num-
drawn upon during the winter by his whole family. Some of ber of direct, physical contacts and stimulation; if the male
the social canids, like the wolves, wild dogs, and jackals, have and female parent swap periods of nest attendance, the nest
well-developed fatherhood roles. An average pack of wild temperature y,iIl be higher and more stable than if one parent
dogs might consist of four or five males, all brothers, and a had to come and go; and perhaps prolonged exposure to male
single unrelated female. The female bears a large litter, of
about a dozen pups, which the adults feed either by the males
regurgitating food to the nursing female or by all the adults
regurgitating to the weaned pups. There is even one known
case in which a litter of Cape hunting dogs was raised entirely
pheromones might have some effect.
Whenever these different forms of male parenting slow
down the male reproductive act, they bring the cycles of the
two genders toward a common rhythm, into synchrony. The
rate at which males rejoin the mating population after repro-
I
by the males in the pack after their mother died. Males in a ducing falls drastically. The population of competing males
family of monkey species that includes the marmosets and the shrinks and fem ales lose their leverage.
tamarins often carry their young through the trees, groom One group of animals in which this can be seen is the
them, and have been seen giving their young food, though it sticklebacks-small, temperate-zone and subpolar coastal and
is hard to know how significant this behavior is. Paternal care river fish. They are carnivorous and eat a wide variety of
has been seen in several dozen rodent species, of which the worms, daphnia, cyclops, fly larvae, and small crustaceans.
beaver is one example. Two zoologists who raised and watched One of their favorite foods is fish eggs, particularly the eggs
some pairs of deer mice (Peromyscus leucopus) report that at of other sticklebacks. The males have taken on the task of
feeding time the males often: protecting the eggs fertilized by their sperm from the ap-
petites of their cannibalistic colleagues. They do this by first
. . . remained in or near the nest while the female alone 0c- building a nest out of vegetation, gluing it together with a
cupied herself with the food supply. At such times the male
might remain watchfully alert or he might, if near the young, kidney secretion, and then shaping it properly. A female ar-
pull the nesting material over them, hover over them, or even rives (we will return to the courtship procedure later) and
wash them. Often he remained with them for as long as five min- lays her eggs in the nest. The male fertilizes them and flat-
utes while the female fed. . . .TO tens the egg mass into a sheet against the bottom of his nest.
He then reshapes, repairs, and lengthens his nest so that the
Studies with paternal-care rodent species have shown re- next egg clutch will no more than partially overlap the first
peatedly that pups reared in the company of both their mother one, like shingles on a roof. Males can fertilize, flatten, and
and father survive better and grow faster than those reared by overlap up to seven clutches over a one- to two-day period.
their mother alone. One such study, done with a predatory. After a few days the male begins to aereate and ventilate
highly aggressive desert mouse (Peromyscus caJifornicus) found the eggs by fanning water through the nest. He inspects his
that daughters tended to be more active and exploratory, and clutches constantly and will pick out and eat any eggs that
sons more aggressive, if they had been raised by both par- die and become moldy. As development progresses and the
ents. Progeny raised in single-parent families were also eggs generate more metabolic heat, the male makes holes in
slightly less efficient at killing and eating crickets, an im- the roof of the nest, almost certainly to enhance the nest's
portant food source for these rodents. The researchers suggest ventilation. Eventually he tears the nest apart and leaves the
three reasons why a paternal presence might have these effects: material piled up in a tangle in which his newly hatched fry
secrete themselves. (The eggs hatch after seven to eight days.) Which really makes one wonder just how much the "idealized
Fry that swim away from the nest get sucked up by the male sequence" itself is worth.
and spat back into the nest pit. Males guard their fry in this Now why should the female decorate her abdomen and
way for about a week after hatching. It has been found that display it to the male? And why should he be interested? As
sticklebacks raised without a father are extremely timid com- female sticklebacks grow, the size of their spawn increases by
pared to normally raised sticklebacks. "Overfathered" fry, an order of magnitude, from twenty to thirty eggs to three
fish kept in the presence of their father for longer than normal, hundred to four hundred eggs. Obviously a male would prefer
are much bolder than normal fish, or at least less responsive, to mate with a female carrying a larger set of eggs. But why
when a predator like trout is introduced into their tanks. should his preferences be given any weight? Why should
Facts like these may be taken as a kind of indirect testimony females be selected to recognize and respond to an aspect of
to the effectiveness of male sticklebacks in providing protec- the male value system? The only reason plausible to me is
tion for their young. that sometimes female sticklebacks have to compete among
Stickleback courtship is unusual in the distinct, if small, themselves for males, and the females that were capable of
role that females are called upon to play. Both sexes develop advertising their virtues properly attracted the right kind of
courting colors. The males' are more conspicuous: their throat males sooner than those that didn't, and that difference mat-
and forebelly turn red; their irises, green; and their back tered.
develops a greenish tint. But females also begin to show Male parenting brings the male and female cycles into syn- (
speckles of dark pigment on their abdomen. These spots chrony both by slowing down the turnover of males and
make her abdomen glitter slightly. speeding up that of females. A large female stickleback who
When a female is ready to spawn, she leaves her school, is lucky in her hunting for food can spawn every four or five
out in deeper water, and swims toward the males' territorial days over a sixty-day breeding season-if she is able to find
areas. When a male responds he does so by approaching the males when she wants them. Further, from a female's point
female in a characteristic, zigzag dance; she "replies" by of view, not all males are equally good father material. The
floating vertically, head up, and orienting her abdomen to- larger a territory a male can maintain around his nest, the
ward the male. This makes her silvery, speckled belly, already less he will suffer from egg-robbing by other sticklebacks.
swollen with eggs, especially prominent. The male then Even if a male defending a small territory does not actually
"leads" the female back to the nest and points to the entrance lose any eggs, the efficiency of his fanning declines since he
with his body. She pushes into the entrance and the male then is so distracted by the presence of neighboring males. A fe-
induces her to spawn by butting her gently on the flanks. If male might therefore be expected to prefer, if she has the
the female is very ripe she can skip the courtship sequence choice, males formidable enough to keep their neighbors at
altogether and simply swim straight into the nest. In fact bay.
stickleback courtship is extremely flexible in all respects. One However, stickleback males, attractive or no, can brood
of the leading students of this fish, R. J. Wooten, describes no more than seven clutches at once. As a rule one would not
the courtship sequence, much as I have given it here, though expect this to be an important limitation on female reproduc-
in more detail, and then says, ". . . occasionally a courtship tivity; in nature, on the average, males seldom reach their
is seen which almost exactly follows this idealized sequence." limit. But it would be surprising if they never did. When food
is ample a large female can spawn two to three times faster attractive in some other way. They probably have small ter-
than a male can run through his nest cycle (males build up ritories and so have little to offer a female but flashiness.)
to five nests in a season, according to observations made under One of the clearest indications of male leverage is females
laboratory conditions, which often bring out optimum per- fighting with each other. In tlie Neanthes caudata, a bottom- I
formances). It seems perfectly plausible that some males, dwelling marine worm in which the male incubates the eggs,
some of the time, will find themselves in a position to pick females are intensely, even mortally, antagonistic of each
and choose whose eggs they are going to brood. Once this other, but tolerant of males. Male emperor penguins incubate
happens female attractiveness suddenly becomes an issue, and the pair's egg over the long Antarctic winter inland, while
females would evolve makeup with which to decorate their the female returns to the sea to feed. Whether a male will
abdomens. To attract males the females obviously have to succeed in this strenuous chore (chill factors can fall down
communicate in the terms males are interested in, and what to a hundred below and more) depends on his fat stores; if a
stickleback males care about are lush, ripe bellies, stuffed male gets too thin he will simply kick the egg away and try to
with eggs, and promising a wealth of paternity. get back to the ocean. A big, fat male is thus a creature of )
Male leverage appears at other points in stickleback mat- great worth and females have been seen to fight with each
ing behavior. Occasionally populations of sticklebacks are other for males with, as the French biologist observing them
found in which the males have abandoned their green and has said, "la grandeur."
red courting colors and are a cryptic black or drab silver. In What appears to be male incitement of female competition
one lake in Washington, only 15 percent of the samples taken has been witnessed in Wilson's phalarope (Phalaropus tri-
were "normally" colored. In laboratory experiments it has been color), a graceful, sandpiperish marsh bird that breeds in ag-
clearly shown that if females are offered a choice of males to gregations on prairie wetlands and Arctic tundra. The males
approach, they prefer the red and green ones. Obviously in provide almost all the incubatory care. Most hens breed once
these populations the predators had sufficiently decreased the and have weak pair bonds with their male, but some manage
population of adult males so that five out of six (in the Wash- to find or attract more than one male who will accept their
J ington example) were able to ignore female preferences al-

together! In most species, needless to say, males can't get away
with doing things like that. If a certain color scheme is im-
eggs, so that some females are excluded from breeding al-
together.
Phalarope females are larger than males, more brightly
portant, either in systems of female choice or male competi- colored, and highly aggressive among each other in the pres-
tion, then the males have to stick to that scheme, regardless ence of a male. Females court males by attaching themselves
of the consequences. An inconspicuous male might lead a long to one and then following him about, all the while threaten-
life, but it would be a celibate one. In the case of the stickle- ing or attacking any other female that approaches, or is ap-
backs, though, the males have more than their usual influence. proached by, the couple. In one series of observations court-
If predators reduce their numbers even a little, which further ing females were found to spend 80 percent of their time in
increases the leverage of those that remain, the combination hostile interactions with other females. (Do the males deliber-
might be enough for males to get away with denying females ately test their females in order to acquire the best mate?)
whatever services bright courting colors perform for her. Often females will fly after any unattached male that appears.
(Prediction: I bet those males that carry courting colors in Sometimes males that are being pursued in this way will swoop
) generally cryptic male populations will be shown to be un- down over swimming females, drawing them into the chase.
These males then stop and hover and the pursuing females more active role in these close-range interactions. She would
fight among themselves in midair as he watches. "Hovering jump on the male or place her front feet on his back and gently
males almost always give 'Courtship Ernts,' " one ornithol- prod his back and vent region. Sometimes the female Would
ogist reports in describing their vocalizations, "the same call climb across the male or sit on him and drum her hind feet
which provokes interfemale aggression on the water." 71 on his back. . . . I never saw a male climb on a female's
back. . . . Sometimes a female would crouch in front of a
Female fighting has also been seen in Dendrobates, the
male and encircle him or rub her head on his chin . . . . As the
frog in which the male carries the tadpoles about on his back. pair moved through the leaves, the female usually became mOre
(Male Dendrobates have also been seen fighting with each active in jumping on the male as courtship progressed.
other, though perhaps that was over a different issue than
[
mate competition.) Dendrobates females have been observed Sometimes a male can be seen leading a whole suite of
eating other female's eggs, which if it is a technique for freeing females behind him.
up parental males, is another form of female competition. A Wells believes that what the female is doing is communicat_
female button quail, a species in which the male does the ing her schedule to the male so that he will know when her
incubating, has been seen attacking a clutch of eggs being eggs are ready to be deposited. She is, as it were, counting
brooded by a male. Male Neanthes caudafa, the patemal- down for him, just the way it is done at Cape Kennedy. From
care marine worm mentioned earlier, tolerate females until the male's point of view, this allows an efficient mating; he
they begin brooding, at which point they attack approaching will not be wasting his time with females that are still involved
females. If they do this because female cannibalism is a threat in the preliminaries of their schedule. Generally all males
to their brood, then that cannibalism might be aimed at free- would like this information; there are a number of mammalian
ing up the male as much as acquiring some rich protein stores. males that acquire it by tasting and decoding elements in the
Both, in this system, are valuable resources, and infanticide female's urine-but they have to do all the work themselves.
might be selected for exactly the same reason it was among Only the Dendrobates males can force the females to tell them
langurs. explicitly. The reason (Wells thinks) is that their mating sys- \
Female fighting is not as common as a greater willingness tem evolved in a context of female competition: Males Were \
by the females to pick up some of the burdens of the mating in a position to pick those females who made matters easiest
interaction. Robert Trivers, who more than any other biologist for them.
has alerted naturalists to the importance of "male parental Males of the bird-of-paradise family (peacocks, bower_
investment," has pointed out that female courting, and bright birds) are usually promiscuous and offer no parental Care.
female colors, are found in some species of seahorses and They are famous for their elaborate courting plumage. But
pipefish. Wild dog females seek out and court the male "broth- there are three species (genus Manucodia) in this family in
erhoods" of wild dog packs. Kentwood Wells writes, describ- which the two sexes form pair bonds and the males help raise
ing the courtship of the Dendrobates frogs: the young; in these species the se ook alike which suggests
Courtship began with a female approaching a calling male a more equitable distribution of these burdens. Pigeons are a
monogamous species in which males parent. In fact, male
\
and sometimes touching his snout with hers. The male would
then move off through the leaves with the female close behind.
. . . As a pair moved through the leaves they engaged in bouts
of tactile courtship. In every instance, the female played the
pigeons even have the ability to make milk, in a gland in
the esophagus, with which they feed their young. (Male ring
doves and emperor penguins have the same capacity. So do
)
female pigeons.) Mate-choice experiments, in which male and
female preferences were deliberately pitted against each other,
Male Leverage and Equality
which the sexes should have equal degrees of influence over
each other, but which look like female-leverage species.
/ 169
(r
showed that females settled for a nonpreferred male sooner Pigeons are an example; the male takes the initiative in pair
than males settled for a nonpreferred female?' Again, this is formation, does most of the courting and has slightly more
an illustration of male leverage, or at least, substantial direc- colorful feathers, despite his paternal nature. There are three
tion away from the usual mating situation, in which males are reasons why one might see this. First, there might be fewer
glad to get any female they can. Very few males, among females than males, so that males are in a poor power posi-
species generally, are ever in a position to define and respond tion regardless of how much they contri?ute. to the offspring.-
/ to issues of female attractiVeness, of differences among fe-
males. These mate-choice experiments show that in a few
Second, the monogamy might be an IIIUSlOn. Males might
be able to have more mates_perhaps throug~ haVing a longer
species males can define and adhere to standards of mate reproductive life-than females, and so WIll come into a
polygamous competition with each other, regardless of how
J) selection-and they can do this because their household tasks
keep them out of competition with each other.
Just about as many female deer mice (Peromyscus leocopus;
paternally they act toward their progeny. Or the males might
be mostly monogamous but competent, if c?nditions alter, to
the paternal-care rodent mentioned earlier) are caught in take up polygamous habits. An exam~le m the cichlids, a
traps baited with male pheromones as males in traps baited fish known for its monogamy, pair-bondmg, and male parent-
/ with female scent. This shows that each gender is equally im-
portant to the other; each works equally hard to solve the
who-where-when problems of mating. Courtship is dramat-
ing (in some species both parents produce a nutritious slime
on their body surfaces from which their fry can feed when
hungry). Usually the male role is .centered aro~nd protecting
the young from predators, especIally other clchlids. Some-
ically evenhanded:
times a male that is already mated to one female may be seen
The two animals chased one another, traveling in head-to- courting a second female as he patrols the borders of his ter-
tail formation with either animal in the lead or with both animals ritory. Evidence like this SUggests that if a male perceives a
simultaneously leading and following as they ran in small decline of interest in the local predators, a lessening of the
circles. The chasing was interrupted by intervals of standing on
threats to his own brood, he will then try to acquire a second
their hind legs, front-to-front with noses touching, and of
nuzzling one under the body of the other. As they moved under mate. Cichlids look alike but the male is larger than the
one another there was more naso-nasal touching and nose-to- female. Larger males are not the usual pattern in fish; the
genitalia exploration as well. They often turned over together, pattern hints at a certain degree of male competition.
sometimes venter to venter, appearing to wrestle gently.. . ." The third possibility why an equal-partner species might
look like a female-leverage species is c~mpletely untestable,
The two sexes "courted" not only when they were strangers but ought to be at least mention~d. It raIses .the thorny ques-
introducing themselves to each other but after the birth of a tion of what sorts of units eVolutlOn works WIth. Suppose that
litter, and after the female was returned to her mate from
• There are a number of species of hole-nesting water fOWl in which the
being removed for a laboratory procedure of some kind. males are not colored cryptically while the females ~r~ •. despite these being
Males did "call" more than females, which is believed to monogamous species. Entirely apart from the POSSlblhty that camouflage
may be less useful to a male (whO doesn:t nest in . the ha,le) several studies
represent a slightly greater effort toward mate attraction. show that females in many of these species are dlfferenltally vulnerable to
There are a number of species that are monogamous, in predators, which gives the survivors leverage.
170 I WHY MALES EXIST Male Leverage and Equality / 171
the behavior or structures that we now see being used in court- The male then [raised] his crest feathers . [until] the
ship originally evolved because of their usefulness in some colored areas of skin posterior to his eyes were maximally ex-
other context-like territorial defense. Then it might be that posed. He wagged his cocked tail from side to side, while
these displays could. be drawn upon for courtship purposes rapidly stepping or patting his feet in place. A rapid, vocal
just because they were available, in preference to developing kuk-kuk-kuk-kuk accompanied this. After a short period of
another vocabulary. In that case while it might appear that wagging and stepping he made a deep bow in which the tip of his
tail nearly touched the floor. . . . A low, almost growling coo
males of such species were taking the lead in courtship, the
was made during the bow.
"reality" is that the world has trained them to act out their
feelings in more expansive and energetic terms than the fe- All this time the male continued to hold the mouse in his
males. But if we could assess the emotional states of both beak; not until the copulation was over was the food given the
animals directly we would find that they had the same at- female. While, in this specific case, the mouse probably served
titude toward each other, whatever that attitude might be. as a cosmetic, as a way of riveting the female's attention to
One route by which male parenting is thought to have the male, it is easy to imagine this behavior ending up as mate-
evolved is via that ancient evolutionary dynamic-female feeding, blue-tit style, assuming only a context of male com-
choice. Females, this theory proposes, have some way of petition.
knowing which male will make the best parent and they have One species that has gone a little further down this road
exercised their leverage to select for that quality. The paternal is the eastern scorpion fly (Bittacus apicalis) , which has been
behavior for which this idea works best is female feeding, the subject of a masterful study by Randy Thornhill of the
bringing the female a meal which is then turned into egg University of New Mexico. The scorpion fly lives in the lush,
protein. This can be an important source of food; one orni- dense undergrowth of the moist, deciduous forests in eastern
thologist found that a female blue tit that begs food from her North America. There it hatches, hunts (by pouncing on other
mate (when her mate approaches with a piece of food she flies, like house flies, in the air and then sipping their fluids),
stops foraging, shivers her wings, and calls) gets 250 percent breeds, and dies in the early summer. Both males and females
more food than does a solitary, self-sufficient female that hunt for the first two or three days after they emerge, but
never begged from males. (The reason for the large return to when breeding season begins the females stop hunting and are
begging is that the food items brought by the blue tit males are fed entirely by the males. When a male captures a fly he first
larger than those taken by females foraging on their own.) tastes it briefly, and then either discards it and hunts down
It seems easy to imagine how this kind of parenting might another, or lands on a twig, elevates his abdomen, and calls
have grown out of female choice. There are many species in for a female by emitting pheromones. If a female responds
which males use food to attract the female during courtship. she lands beside the male and lowers her wings. He presents
William Calder of Duke University described such a court- both the fly and his genitals simultaneously. The female tastes
ship among captive roadrunners (Geococcyx californianus): the prey-Thornhill calls it the "nuptial prey item"-which
A mouse given to one of the males often seemed to act in- continues to be held by the male, and either feeds from it or
stantly as an aphrodisiac. . . . Bearing this food, the male flies away. Only the female feeds during the copulation.
went to the female, usually approaching from the rear. Sometimes Thornhill found that the flies discarded by the males tended
the female begged like a roadrunner chick, fluttering her wings to lie in the smallest third of the prey-size range. He also found
and uttering a buzzy, squeaking call. that the length of the copulation, which could proceed for as
long as twenty-five minutes, seemed to correlate directly with calls, and after which she becomes receptive again and rejoins
the volume of the "nuptial meal." When a male tried to the mating pool. She might mate four times in a day. Males
present a female with a fly that measured less than 20 mm', need about fifty minutes to find a prey of an acceptable size
she would either refuse to copulate at all or break away after (to establish this point Thornhill individually marked forty-
just a few minutes. two males and followed them, stopwatch in hand, as they
hunted), and this limits their mating opportunities to about
One male presented a [fly) 10 mm' to an attracted female.
The female began to feed on it, but each time the male attempted ten a day. Thus, assuming that the females are so efficient in
to copulate with her she pulled her abdomen back, thereby finding males that they enjoy their maximum possible ad-
preventing copulation. After about one minute the male pulled vantage, their edge will be four to ten or one female to two
the prey from the grasp of the female and presented it to her and a half males. This still puts them in a powerful posi-
again. The female again refused to copulate and after another tion, but there are many females in nature that play from a
minute the male grabbed the prey from the female and the pair much stronger hand.
parted. . . . within four minutes [the female) had coupled with The scorpion-fly sex system is rich with signs of emerging
another male which possessed a nuptial meal of 20 mm'. This male leverage. First, the male does not go looking for the
copulation lasted twenty minutes and was terminated by the female; she flies to him. He does not even have to distinguish
male. In the second reproductive encounter the female showed the genders; the female identifies herself. In fact, a whole class
no signs of coyness and coupled with the male after tasting the of scorpion-fly male parasites have evolved that make use of
nuptial mea!.'"
this male dependence on female courtship. These "transvestite"
Thornhill found that for the first five minutes or so of the males, as they have been called, follow up pheromone calls,
copulation the females prevent any sperm from entering their land next to the calling male, lower their wings just as the
body. After five minutes the number of sperm permitted to female does, and grab onto the fly when the male extends the
enter climbs rapidly for twenty minutes, after which the in- prey. Of course they do not couple; they keep their genitalia
crease flattens out. At this point the male usually breaks off just out of the reach of the calling male. After a few seconds
relations. The male and female fight over what remains of the it usually dawns on the calling male that something is wrong
fly, if anything does. If the male wins he examines it once and he then tries to snatch the fly back. But by this time the
more, and then either calls for a second female or discards it transvestite has gotten a firm hold on the fly and sometimes
and begins hunting again. The female then retires and im- suceeds in wrenching it away from the male that originally
mediately lays an average of three and a half eggs. caught it. The robber then flies off and uses the stolen fly as
There could hardly be a clearer illustration of the influence bait for females for himself.
of female choice on the evolution of male parenting. Yet logic Male parenting need not, however, depend on female choice \
argues that as important as female leverage is in other con- and male competition over numbers of mates to drive its
texts, it can have only limited usefulness in forcing the evolu- evolution. A hunting insect like a scorpion fly cannot conceal
tion of male parenting. The trouble with male parenting is itself from predators as easily as can a vegetarian insect,
that it takes time, and reproductive acts that take time destroy which can hide under leaves or burrow into stems. Thornhill
the whole basis on which male competition is built. The does not describe the intensity of the risk that scorpion flies
scorpion-fly female lays her eggs over a four-hour period, undergo from birds while they cruise about looking for game,
during which time she is unresponsive to other pheromone but since they live in a bird-rich habitat, and have their popu-
lation peak during a period when many birds are breeding, beetles sequester large pieces of food that are usually fought
there is nothing implausible in assuming that the risk is high. over by several beetles. Any male that fertilized a female
If so, then males that fed the females that they mated with, and left without helping defend and bury the carrion would
and thereby allowed them to keep out of sight while laying have no prospects at all. The cichlids and the sticklebacks live
those eggs that carried the males' sperm, might outcompete in environments that are fiercely hostile toward their progeny;
males who do not give gifts and force their females to fly parent-removal experiments show that the fry get eaten up
around hunting for protein. The risk to females, and there- within minutes after they have lost their parental protection.
fore the gain to males who kept their mates out of sight, would (I know of no experiments in which only the male was re-
have to be large, but perhaps it was large. In other words, moved.) Male parenting is also found in many tree-dwelling
depending on the situation, male competition alone can drive species--many birds, and some arboreal primates, in which
males into forming cooperative relationships with specific the males carry the young. It seems plausible that in these
females. In the situation envisaged here the scorpion-fly males species it is important for the female to be light, and that
are not (only) competing over the number of females each value selects in tum for early deliveries, for her young being
can fertilize, but over who can get the most potential off- born'e long before they are large enough to take care of them-
spring past that critical moment when the mated female is selves. The addition of male care might make an especially
vulnerable to predators. Depending on how important that important difference in these conditions. Among birds gen- [
competition is, females will not need to exercise any choice erally a lack of male parenting seems to be associated with
at all to get themselves a provider. In fact, to push the argu- food that does not need to be caught. Promiscuous species
ment to an absurd extreme, males in such a system might be tend to eat nectar and fruit, which, when available at all, is
selected to force-feed females if necessary, not that it ever abundant; polygamous species tend toward seeds and plant
would be. In this context male parenting can evolve even when food; while monogamous birds tend to eat insects and other
the pool of competing males is comparatively small; female animals. It may be that in flesh-feeders the amount of food
/ leverage is just not relevant. returned to the nest can make a big difference in the num-
Much of this book has tried to imagine ways in which the ber of offspring successfnIly fledged, while in the other spe-
apparent paradox of the nonproductive male might be seen cies the young already get enough food; what limits their
as making evolutionary sense. To the degree that such ideas number is some other factor (such as the brevity of the fruit-
seem plausible they raise questions about productive males. ing season) about which males can do nothing. In some
What causes males to give up chasing and competing for fe- species of flesh-eaters, like gulls, one parent is needed to
males? And why should females ever be selected to give up stand guard at the nest against the attacks of other members
their leverage and put themselves in a position to have to of the species.
respect male needs and values on the who-where-when-how Even if a male doesn't play a critical role in reproduction, \
issues? he will be selected to contribute to his offspring if he has
It is easier to see what causes males to "settle down." nothing better to do anyway; if circumstances prevent his
Paternal males, where they exist, usually play critical roles competing over more females. This might happen if the fe-
in the reproductive cycle, and it is easy to imagine that a males are dispersed widely, or pass into and out of estrus too
promiscuous male, under those conditions, would lose all his quickly, for him to be able to visit more than one. Or it might
offspring, no matter how many he fathered. The burying be too dangerous for him to move around. The elephant
shrew (Elephantulus rufescens) is a small insectivore that This is a good example of the advantage to females of a
has adopted, as its main anti predator strategy, flight. It main- polygamous system. The good territories are open to more
tains a maze of cleared pathways within its territories down than one female, and the males have been selected, by virtue
which it zigs and zags when being chased, for example, by a of their competition, to advertise the quality of their territories
snake. Males and females share a joint territory and nothing in a convenient, easy-to-read, summary form. Thus the fe-
else. They do not sleep or rest together, or court, feed, or males can choose, resources or paternal care, whichever prom-
even groom each other. Since the males do not have to main-
tain the level of protein intake the females do, they have,
relatively, some time free, and they use that time to keep the
ises the best results.
Male parenting is thought to evolve in environments that
are ecologically stable and (therefore) socially competitive,
1
system of runways clean. They spend twice as much time habitats in which excess population growth is cut back by
maintaining the escape routes as the females. While it might competitive interactions among the members of the species.
be argued that this kind of male parenting could only make a These are the circumstances in which each new increase in
slight difference to the male's reproductive success, it would male care is likely to be strongly rewarded, since very small
make more of a difference than anything else he might do initial advantages in size and/ or training of the young can
with his time-he's certainly not going to abandon his run- determine who wins these encounters, and do so over and
way network to roam around looking for females-and that's over. A small edge early in life can, if the rules stay the
J what counts.
So one can imagine selected, special cases in which male
same, snowball to a large payoff by adulthood. Male parent-
ing allows the young to stay young longer, and therefore
parenting might be adaptive for males, but what about fe- to bring more to the business of being adult-whether a larger
males? Why should they prefer goods to service? Why suffer size, a more developed nervous system, or a better s~nse of
the inconveniences that attend their giving up their leverage the environment-when they do finally go off on their own.
over males? In general the freedom of choice seems to be The examples of male parenting given here have tended to
important to females; why should they be willing to give it stress the protection of vulnerable young, and certainly when
up? Some females do in fact reject male parenting; there are one sees progeny being threatened by predators several times
species of marsh birds in which the males do feed the young their size, that seems the most sensible interpretation. But at
and perform other functions. Yet even so the females some- least in some cases, especially in some bird and mammal spe-
J times prefer to nest polygamously, with two or so females to cies, one wants to ask why the young are born so vulnerable
a territory. This dilutes the amount of care the territorial male in the first place and then take as long as they do to reach
can give, but if his territory is rich enough the females will adulthood. It can be argued that when all the juveniles in a
prefer to live there rather than accept the assistance of a given generation are going to be forced to compete with e~ch
male in a poor territory. Studies have shown that the terri- other over a very limited number of nest sites, or foragmg
tories of bigamous males are both larger and contain more territories, when the main barrier between them and success-
standing water (wrens feed on aquatic invertebrates). They ful adulthood is not huge predators but each other, then pro-
also have more male-built nests; the investigators suggest that longed immaturity and, consequently, vulnerability might
the number of nests a male builds is an index of that male's actually be selected. Offspring tolerated by their families for
) territory's quality, since a male that could build many nests any length of time are so treated because it is to everyone's
obviously needed to spend very little time looking for food ...• advantage that they learn as much as possible about the world
and how to live in it. One way of giving them a "head start" including the specialization of gender, are adaptations to so-
is to get them born and into an environment that is both more cial competition, to living in a species that prunes back its
open to the world, and still protective. H there are any ir- own excess population growth. The advantages of size flow
revocable decisions that have to be made about how adult life from its usefulness in direct competition, "when push comes
is to be entered and practised, then it is better to postpone to shove"; of specialization, in the indirect competition of
these until adulthood is in fact at hand and the conditions efficiencies. A specialized forager will crop its habitat faster
of the moment can be examined. Schelling, the nineteenth- and closer than a less specialized peer. It is possible that male
century German romantic philosopher (who wrote on bi- parenting is a way of enhancing both these modes of social
ology), believed that the position an organism occupied on adaptations at once, or alternately. A period of protected
the scale of life, the great chain of being, depended on how immaturity allows the young freedom from worrying about
long it had managed to delay sexual maturation. Once a crea- the two priorities of adults-survival and reproduction-and
ture became sexual its fate was sealed, Schelling thought, or they can, instead, put all their energies into learning and
at least defined. Lower organisms were those that had suc- growing.
cumbed to temptation and indulged in sex at an early age. From the female's point of view male parenting might well
While they may have enjoyed themselves at the time, they be a net benefit, but it is hard to believe that there are not
paid for it, because they were forever frozen out of the chance some costs to her in accepting it. One would think that the
to ascend to the higher levels of organization, and had to mating system would have to become more sluggish and less
trudge through life as a worm or a plant. Organisms with the convenient. She has become dependent on another creature
self-restraint to postpone sex, postponed with it its rigidifica- for an important part of her reproductive cycle. The male
tion and commitment. might compete with her for resources. In many species the
While Schelling's ideas in their original form have little female mates repeatedly with the same male, and this will
but entertainment value for the contemporary reader, they clearly restrict the genetic variability of her offspring. And
do hold a grain of truth, which is that keeping one's options male-parenting systems generally require females to be more
open till the last possible minute makes good sense. When sensitive to male needs, because the pool of competing males
paternal care makes this possible, then the association be- is less likely to be a factor.
tween male parenting and offspring dependency will be The silver lining in all this, one supposes, has to be male
strengthened. Finally, paternal care allows progeny to de- care. There might be a second advantage, springing, iron-
velop adaptations that need practise and polish to be useful. ically, out of one of the apparent disadvantages of male
One might imagine, looking at the halting, callow, incompe- parenting, which is the dependency of the female on the
tent manner in which a young fox pup hunts, that male male. Seriously dependent relationships, apart from those of
parenting evolved because fox puppies are so vulnerable and the young on the parent, are uncommon in nature, at least
dependent-but in fact it is just as easy to argue that a pro- among sexual animals. Symbiotic, mutual-benefit relationships
tracted period of dependency is a great plus in evolution, that are not rare, of course-the birds in a flock increase their
foxes could never hunt as well as they do without having a foraging powers by combining, or starlings amplify their de-
part of their lives devoted explicitly to studying and prac- fensive powers by flying in groups (they bunch together when
tising the craft. a hawk flies overhead; this makes it harder for the hawk to
Earlier it was argued that both size and specialization, strike at one starling without inadvertently colliding with a
\
180 I WHY MALES EXIST Male Leverage and Equality I 181
second, which, at the velocities hawks reach in their dives, very few species in which rape has been observed), the fe-
would be likely to seriously injure the raptor). But these male's mate intervenes aggressively about one-third of the
intraspecies symbioses tend to be fairly loose; they are neither time, usually by grabbing the assailant by the neck and beat-
highly elaborated nor do they turn on the competence of ing him with his-the male mate's-wings. (One reason why
specific individuals. The ordinary sexual relationship is an the males intervened only one-third of the time was that mal-
\ example. Females are not dependent on males for anything lard rapes are usually committed by multimale gangs; the
but the performance of a routine that can be acted out by mated males were only half as likely to intervene when their
all males interchangeably (and they might accept mUltiple female was being assaulted by a gang as when she was at-
fertilizations in addition); successful males mate with many tacked by a single male.) After the rape about one-third of
females, which makes them less dependent on the luck or the mated males copulated immediately with their mates,
competence of any single one of their mates. skipping almost entirely the usual precopulatory displays.
Male parenting involves a quantum leap in the degree of Barash believes this is an anti-cuckolding trick; an attempt
interdependence experienced by the partners. The females in by the mated male to compete with the sperm introduced by
such species depend on specific males to perform their paternal the rapist. Mallards are essentially monogamous; males are
role, while males commit their reproductive prospects to a dependent on a single female to bear their progeny. This de-
small number of females, perhaps to even just one. There pendency leaves them vulnerable to cuckolding and makes it
are exceptions. The stickleback and the scorpion fly combine necessary for them to defend their mates. Barash believes that
male parenting and high degrees of mutual independence by one reason why these hasty copulations did not follow rapes
breaking up the breeding season into many reproductive in every case is that mallard females can tell whether sperm
cycles. A third example is the American rhea, a ground- was transferred during a copulation and so can inform her
nesting Latin American bird. In the spring the males com- mate whether or not a rape did constitute a genuine threat
pete among themselves to acquire "harems" that range from to his paternity.
between two to fifteen females. Each male builds a nest, and In another series of experiments, Barash placed model male
all "his" females lay in that nest until the clutch has built up mountain bluebirds (Sialia currucoides) on the nests of mated
to a few dozen. Then the male (apparently) drives the fe- pairs while the male was out foraging. He found that when
males away and begins to incubate the eggs. The females go he did this before the female had laid her eggs the male at-
off to consort, copulate, and lay eggs in the nest of a second tacked both the model and his mate (he "pulled an un-
male, and might in a single season lay in the nest of as many determined number of primary feathers out of his mate's
as seven males. While the rhea mating system may not have wing . . .") and then drove her away, replacing her with
evolved for this reason, it does allow each bird to hedge its another female. But when he placed the model on a nest in
bets and spread the risk of failure. which the eggs had already been laid the male was much less
As a rule, though, male parenting is more entangling, and hostile to the female.
a number of experiments have shown that this increase in Barash interprets all these results as adaptations by males
vulnerability is serious enough to have evolved its own pro- to their being dependent for a major fraction of their pro-
tective devices. David Barash, a psychologist-zoologist at the creativity on one female. The male mountain bluebird drove
University of Washington, reports that when female mallards away the female that, appearances suggested, had been fer-
are "raped" by strange males (the mallards are one of the tilized by another male, because if "his" female had laid
eggs not fertilized by him he would have been co~pletely partner will be adapted to enhance the performance of4he
shut out of reproducing that season. Male mountalD blue- other almost as strongly as it will be to improve its own.
birds have leverage; they seize and defend nest sites, which (I say "almost" only because the loss of one parmer and
are in short supply. The male bluebird could therefore afford then pairing with a new one is likely to be part of any ani-
to drive his adulterous female away. Male mallards have no mal's experience, no matter how tenacious their pair bond.)
leverage and therefore have to settle for the more proble- If these parmers associate with each other continuously, then
matical strategy of physical intervention and sperm competi- they will have both the incentive and the opportunity to de-
tion. vise individualized, particularized accommodations to each
A third experiment pointing to the same phenomena was other's qualities that act to enhance the reproductive efficiency
done at Duke University with pairs of ring doves (Strep- of the pair as a whole.
topelia risoria).'· Two groups of females were used; one com- The classic study of this effect was made by J. C. Coulson,
posed of female doves that had previously been courted by a zoologist from the University of Durham in Great Britain,
males and the other of females that had been isolated from Who studied a colony of kittiwake gulls (Rissa tridactyla) for
males. Male doves were placed first with one group of eleven years. He found that females that changed their mates
females and then, a few days later, with the second. The fe- did not lay as early in the season, laid smaller clutches, and
males that had been courted already gave a more advanced despite having fewer eggs to look after, hatched fewer eggs.
response to the displays of the males than did. the "unex- ''This suggests that the birds in a newly formed pair are less
posed" females. This advanced response had qUite an effect well adjusted to each other," Coulson writes, "that they do
on the mood of the courting males. Overall they were about not stimulate each other to as high a level of reproductive
twice as aggressive toward the "exposed" females and courted drive, and that they cannot coordinate their incubation pat-
them only half as much. "The difference in response may be tern as well as a long-established pair." To give an example,
related to the differing probability of cuckoldry," the experi- he found that a female that changed her mate between breed-
menters conclude. ing seasons delayed laying her first egg by about four and a
These experiments stress the negative side of interde- half days. Even having changed mates a year ago, before the
pendence, the prospec.t, or. reality, of the con~ract b:ing b~o last breeding season, she still delayed egg laying by about
ken. There is a positive SIde, too, and that IS the IDcentive three days. A female that had changed mates for two succes-
to capitalize on the prolonged associations often found be- sive years retarded the date when she laid her first egg by
tween the sexes in male-parenting species to fine-tune the over seven days. These and other negative effects on the kit-
relationship. Ordinarily, when a successful male mates with tiwake breeding biology affected females regardless of whether
many females and a female with many males, then anyone their partner had died or been "divorced," and so were a
mate is, for the other, always just one of a number. Time product of beginning with a new mate rather than the reason
spent fine-tuning one of these relationships is time wasted. for the change. Changing partners is not necessarily a bad
But when two animals mate together repeatedly, so that their idea; a pair that had hatched no eggs at all in one season
procreativity is represented and r~gistere~ by the' sam: set of might profit from a change in partners, and, indeed, two-
offspring, they will, from the POIDt of vIew of evolution, be thirds of the birds that failed to hatch a single egg did "di-
selected as though they were one bisexual organism. Each vorce" and re-pair. Results confirming and paralleling
Coulson's have been found in the red-billed gull (Larus while foraging so as to share whatever discoveries either mem-
novaehollandiae scopulinus Forster) and the Arctic skua ber makes. A second suggestion relies on many of these species
(Stercorarius parasiticus). being "opportunistic breeders," birds that can control their
Work like Coulson's is the strongest argument that pairs reproductive cycle so as to breed at moments that are optimal
can develop partner specializations that allow them to attack ecologically and physiologically. Such pairs might need both
the various issues in their lives, including but not restricted to stay in touch with each other and monitor each other's
to reproductive issues, in a coordinated way. There is much mood. A third explanation is that continuous and individual-
indirect evidence that also points in this direction; evidence ized contact reduces the risk of hybridization with similar-
that suggests that it is important for each member of a pair to looking species. There surely can be no doubt that one of the
communicate more or less continually with the other. virtues of the pair bond is that it does prevent hybridization;
\I The best singers in birds, those with the most complex

songs, tend to be monogamous. From one point of view this
is a little surprising, since one economical way of accounting
no hybrid plumages have ever been recovered from the three
monogamous bird-of-paradise species mentioned earlier. But
that is not to say that the pair bond evolved in the way it did
for complicated birdsongs is to suggest that they evolved under because, and only because, birds with weaker bonds hybridized
sexual selection, just the way peacock displays evolved. Yet more often. A fourth possibility is that continuous communi-
the males of promiscuous and polygamous species, who are cation allows each bird to compare the other's assessment of
most likely to be subject to sexual selection, have compara- the environment with its own, so that an experienced pair
tively simpler songs. Monogamous birds also have the best- might be able to forage, or detect predators, more efficiently
coordinated and most precise songs. These are called duets, in that each member would have access to the "judgment"
or duetting, in which mated pairs keep in contact by calling of the other. The logic of this suggestion works best-the ad-
antiphonally back and forth, the first vocalizing one or more vantage of being an experienced pair is at its peak-if one
notes and its mate instantly responding with a variation of the assumes further that each bird can learn what the strengths and
first call. "So fast is the exchange," E. O. Wilson writes, "some- weaknesses of its partner are, and which responses are more
times taking no more than a fraction of a second, that unless likely to be useful, or right, compared with its own. If that can
an observer stands between the birds or uses sophisticated happen then each bird can learn from the other, can, as it were,
recording equipment he does not realize that more than one grow in the relationship.
bird is singing." Duetting is known in a great many birds, Whatever biologists finally agree on as the point of the
including cranes, sea eagles, geese, quail, woodpeckers, and pair bond, it adds an interesting final twist to the story of
in at least two species of monogamous primates: the siamang natural sexuality. Imagine distributing all living species into
and the gibbon. The talking birds, like the mynahs, parrots, four groups, depending on how important social interactions
starlings, ravens, and others, are all monogamous. It is often are among them. The ideas discussed here would lead one to
observed of pairs in these species that each pair develops its predict that the first group would be composed of creatures
own common call, distinct from those of neighboring pairs, like bacteria, who are adapted to completely unpredictable It.cl";'
through which they keep in touch. Several suggestions have and unstable environments, and who are seldom sexual at all. ,n N~
been made as to the point of these communications. Many of The second group are those for whom social competition ,I"· t
these birds live in dense forests, and perhaps knowing each has become important enough for specializations to emerge, (1<'''''''
other's call allows the two birds to stay close to each other and therefore for parents to profit from an adaptation !Lice sex
that allows them to hand down a wider range of professional asked as to whether mated animals feel love for each other
'\ possibilities to their offspring than they could if they were Obviously this question can never be answered with real
asexual. But the competitive interactions are not as yet so authority; but if, as many people think, love is a sense of de-
important that there is any advantage to be gained in regulating pendency freely entered into and mutually maintained, then
and defining in depth how the issues raised by sex (who, when, arguing that such animals as two old kittiwake gull mates do
where, how) are to be solved. These species are the bisexuals, not feel love for each has to be judged an unwarranted and
creatures that are sexually generalized, that are all identical to uneconomical speculation, with neither evidence nor logic to
each other. support it.
The third point on the scale is reached when specialization
reaches the administration of mating issues. Gender arises,
and with it ranges of specialization and techniques of labor
division that leave the sexes defined in very different ways.
The fourth stage is composed of those species that are so
"well adapted" to their environment that they are seldom
badly surprised by it. Whether they will succeed in breeding
for a given season, or even over their life, is a social question,
I decided by social forces. In such species, large, well-informed
young, whose skills have been brought to a high polish, will,
almost by definition, have an advantage. This requires giving
the young a protected environment in which to grow, and that
\ rc.dneed is both the opportunity and the reward for the evolution
l
W :: J of male parenting. As male parenting develops, one force that
.., I was defining the sexes in opposite ways--their different re-
. . productive tempi-ceases to apply. Moreover, to the degree
l'~""\~' that the protective environment must be continuously main-
tained, so that the two sexes have to spell each other, then a
second force that was defining the two sexes in different direc-
tions, which was a role-segregated division of labor working
within the mating interaction, also ceases to apply. As the two
sexes become involved in the same tasks, as they do the same
things, they will necessarily be selected in the same directions.
The result might look as though the species were becoming
hermaphroditic again, but that is only because the unit of
specialization has moved "up" one notch from single individ-
uals to the pair itself. It is the pair that is, as a whole, selected
to pursue strategies, maximize efficiencies, and interact as a
unit with other pairs, other parents. The question is sometimes
NOTES
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INDEX
adaptive elite theory, 120-127, of, 27, 46

146 description of, 26-27
aggressive behavior, 182 as dominant life-form, 25
in asexual vs. sexual systems, evolution of, 26-27
62 gene characteristics of, 28-30
by females, 159, 165-166 hab itats and, 46, 47
infanti cide as, 129-133, 136- low-energy states of, 28, 46
138, 166 protozoa and algae vs., 35
male competition and, 107- reproduction rates of, 28-29
109, 114, 136-138, 142- sexual reproduction of, 29
143 in symbiotic relationships, S9
alarmone, 54--55 Barash, David, 180-182
algae, 35, 36, 38-39, 51, 59 barnacles, 76, 152
altruism, 54--56, 60-63, 65-66, Bartholomew, George, 115-117
96 Beauli/ul Swimm ers (Warner),
definition of, 60-61 147- 148
kinship and, 62-65 beavers, male parenting by, 159-
amoebas, 3511, 54--55, 60-61 160
amphibians, 41, 100, 113n, 157- bees, sand, 97-99, 112
158 beetles, burying, 154--155, 175
anglerfish 73-75, 152, 154n birds
anis, groove-billed, 59-60 cooperation-competition links
antelope, Africa n, 100, 104--105, and, 59-60, 103
153 courtship displays of, 89, 92,
ants, 62, 63 103-104, 114, 127
harvester, 118-119, 120 duetting among, 184
aphids, 43n, 63 egg wastage among, 59- 60
Armitage, Kenneth, 101-102 female accommodation in,
141-146
baboons, 112, 141 female competition among,
bacteria 165-166
asexual reproduction of, 28- female incitement in, 114--115
29, 30, 185 fight-or-f1ight reflexes in, 93-
boom-or-bust population style 95
202 / WHY MALES EXIST Index / 203
birds (cont.) cockroaches, 36-37, 38 In asexual vs. sexual systems, 59, 76, 79, 109
helpers-at-the-nest phenom- Collias, Nicholas and Elsie, 142- 58-59, 66 Davies, N. B., 113-114
enon in, 63-65 146 competition linked with, 59- deer, red, 108-109
male parenting among, 16, colobines (leaf-eaters), 136-137 60, 66, 68, 103-105, 106, Dillard, Annie, 15
154, 158-159, 167-168, competition, 17, 22, 23-24, 45, 174 dinosaurs, 109
175, 181-182 66, 67, 96-109, 152, 154n, kin selection theory and, 62- DNA, in protista, 36
monogamy among, 133-134, 174 65 dogs, wild, 17-18, 160, 166-167
168-169, 181-185 altruism vs., 61-63 see also organization; parent- doves, ring, 167, 182
opportunistic breeders among, cost to females of, 128-138 ing, male dragonflies, 100, 128
185 in Darwin's theory, 21-23, 61 copepoda, 75-76 ducks, 114-115, 133
parasitic, 153-154 female control of, 110-127, copulation duetting birdsong, 184
size in, 113n 134-136 dominance as goal of, 115- dwarf-male system, 152
vulnerability of young of, female-female, 77, 145-146, 117
177-178 150-151, 159, 163-167 mechanical stimulation of, earthworms, 72
birds-of-paradise, 167, 185 forms of, 17-18 92-93 ecology
bisexuality, 32, 186 gene sets and, 117-118, 119 coral fish, 81-83 dewlap patterns and, 90
advantages of, 71 kin selection theory and, 62- Coulson, J. C., 183-184 excess fecundity and, 45-52
defined, 31 65 courtship displays, 18, 144, 147, exclusion principle in, 48-49
distribution of, 75, 76 limitations on, 111, 123, 139- 150, 162-163, 164-165, gender flexibility and, 78
explanation for, 76 150 168 male parenting and, 177
bluebirds, mountain, 181-182 male aggregations in, 103- aesthetic function of, 127 see also habitat
bonito, Pacific, 114 105, 106 as communication, 86-90, eels, American, 75
bowerbirds, New Guinea, 18, maturation delays and, 106 164 epuresis (enurination), 88
167 mortal battles in, 107-109, as competition, 97, 99, 153 estrus cycle, 70, 110, 111, 112,
Brachionis, 41 137-138, 142-143 endocrine changes and, 92-95 114, 120, 138, 140, 141
butterflies, 22 paternal care and, 168, 172- evolution and, 170 in synchrony with males, 161,
173 female feeding and, 170-172 163
sexual reproduction and, SI- fight-or-f1ight reflexes and, evolution
Calder, William, 170-171 52, 59, 6 1-62, 66, 67-68, 93-95, 106 altruism vs. competition in,
canaries, 92 70, 72, 75, 76-77, 91-92, threats and, 114, 142-143 61-62
cannibalism, 152, 154n, 166 95 cow dung, 48 courtship and, 170
cats, 92 size and, 45-47, 51-52, 113- cowbirds, 153 dependency period and, 178
Chlamydomonas reinhardi, 38- 114, 120, 139, 153, 169, Cox, Cathleen, 117, 121-123, Eastern vs. Western theory of,
39 179 140 27
chronological elite, 146-150 social, 45-47, 50, 66, 103- coyotes, American, 112, 124 female choice in, 170-172
Cichlasoma, 50 105, 106, 177-179, 186- crabs of gender, 67-77, 186
Cichlidae , male parenting by, 187 Chesapeake Bay blue, 146- toward hermaphroditic spe-
155-157, 169, 175 specialization and, 48, 50-52, 150 cies, 186
cloning, see reproduction, 67, 179, 185-186 fiddler, 86, 155 masculinity as alternative in,
asexual vulnerability of young and, hermit, 40 23-24
clovers, 59 177-178, 179 cuckoos, 153 monogamy and, 182-187
clown fi sh, 81-83 see also territorial rights sex as antisocial force in
Clutton-Brock, Tim, 108-109 cooperation Darwinism, 16,20-23,25, 33, (Wilson), S4
evolution (cont.) flocking, 58 kittiwake, 183, 187 see also social insects
sexual maturation schedules food chain, 26 red-billed, 184 invertebrates
and, 178 foraging, breeding vs., 69, 74, gender flexibility of, 78-79
sexual reproduction selected 76, 84, 153 habitat male parenting by, 154-155
in, 34, 44, 52, 67-68 Forel, Auguste, 63 asexual VS. sexual reproduc. males from unfertilized eggs
specialization and, 16, 44, 47 Foster, Mercedes, 93-94 tion and, 39-40, 42-44, 51 among, 119
52, 186 foxes, 178 breeding systems and, 186 see also marine invertebrates
survival theory of, 22-23 Fricke, Hans and Simone, 82 spanadry and, 75-76
see also D arwinism frogs, 72, 85, 92, 103, 106 see also ecology; territorial jacanas, American, 158-159
exclusion principle, 48-49 neotropical, 152, 154n, 157- rights jackals, 160
extraterrestrial bacte rial spores, 158, 166- 167 hadrosaurs, 109 Jacobs, Merle, 128, 151
28 fruit flies, 48-49, 90-91 Halliday, T. R., 113-114 jellyfish, 53-54, 59
fungi, 42, 54-56, 59 "handicap principle" (Zahavi), Jenni, Donald, 159
female feeding, 170-172, 173 124, 127 Jimmy potting, 149
fertilization gall midges, 42-43 Hare, Hope, 62-63, 135 Johnsgard, Paul, 114-115
"chronological elite" and, Galton. Francis, 58 heath hens, 104
146-150 gazelles, 17-18 helpers-at-the-nest phenomenon, Kessel, Edward, 134
laboratory-induced, 72 Geist, Valerius, 17 63-65 kin selection theory, 62-65
fight-or-flight reflexes, 93-95, gender Holldobler, Bert, 118-119
106 defined, 30-31 Hrdy, Sarah Blaffer, 129-133, langurs, hanuman, infanticide
fireflies, 17,70, 103 determination of, 78, 83, 134- 137, 138 among, 129-133, 136, 138,
fish 135 hyenas, 138 166
altruism in, 156-157 evolution of, 67-77, 186 Le Boeuf, Burney J., 117, 121-
asexual reproduction of, 41 flexibility of, 78-83 impalas, 100 123, 140
cooperative assemblies of, 58, gene transfers and, 34 incitement lek systems, 103-105, 106, 118,
103
u+" and .. _" as, 38 benefits to males of, 141 127
courtship displays of, 90, as specialization, 50, 77, 179, in female competition, 165 male advantages in, 139-140
162-1 63, 164-165 185-186 in male competition, 112-115, leopards, 133, 136
gender flexibility in, 79-82 gene sets, 117-118, 119-120 120, 121-127, 136 lichens, 59
male parenting and, 21, 155- gene-copying, in bacteria, 29 individuation life, defined, 15
157, 161-163 gene-labeling hypothesis, 89-90 altruistic sacrifice and, 54-56, life span, competitive mating
maturation delays in, 106 genetic-elite theory, 120-127, 60-63 and, 17-18, 22, 109
parasitic males in, 74, 152 146 evolutionary, 44, 47, 52, 66 Linnaeus, 27n
in reproductive cycle, 21, 69- gibbons, 184 see also organization lions, 100-101, Ill , 133
70, 72, 73-74, 99-100 Gier, H. T. 112, 124 infanticide, 129-133, 136-138 living things
size of, 1I3n Gilbert, John, 42 166 dead things vs., 15
territorial competition by, 100 giraffes, 70 information exchange, 68-70, distinctions between, 35, 41
flatworms, 43 goldfish, 72 84-91, 95, 108, 164, 167, lizards, 141
fiies, 42, 48-49, 50, 70, 85, 90- grasshoppers 184-185 asexual, 43-44
91, 106 American, 18 insects, 49, 50, 75-76, 85, 100, copulating behavior of, 120-
balloon, 134 European, 89- 90 103, lOS, 119. 134, 152, 121
eastern scorpion, 171-174, great chain of being, 178 154n courtship displays of, 87, 88-
180 gulls, 175 male parenting by, 154-155 89,90,92
206 I WHY MALES EXIST Index I 207
lordosis, 93 in nonmating interactions, mollusks, 41, 78 individuality and, 58-60
love, meaning of, 187 139 mongooses, altruistic behavior specialization and, 54, 56, 59
low-energy states, 28, 46 size of, 113n, 120, 138, 139 in, 65-66 see also lek systems
mallards, 133, 180--181, 182 monkeys, 129-138, 160 Origin of Species, The (Darwin),
McKaye, Kenneth, 155-157 mammals, 167 monogamy 20
males courtship behavior in, 92, 103 control reversal and, 152-153 ovipositing, 100
asexually vs. sexually pro- duetting by primates among, efficiency of, 185
duced, 57, 119 184 gender leverage in, 168-170
compensating advantages of, lek system in, 104-105 hybridization prevented by, pair bond, see monogamy
23-24, 33-34, 71, 76-77, male parenting by, 159-161, 185 paramecia, 35n. 40
174-180, 185- 187 175 male parenting and, 167-168, parasites, 78, 135, 173
discrimination reduced in, male vs. female size of, 113n 181 parenting, male, 16, 23, 154-
85-86 vulnerability of young of, among mammals, 65 161, 165, 166, 167-168,
in evolution of gender, 23-24, 177-178 of parasitic birds, 153-154 169, 174
67-77, 179, 186 manakins, 93-95 positive vs. negative aspects ecological factors and, 177
female accommodation to, man-af-war, 53 of, 181-187 evolution of, 170--180, 186
140--150 mantids, 152 moths, 22, 69 experiments with, 180--182
female control of competition marine invertebrates, 75-76, mountain sheep, 17 female responses to, 176, 179
among, 110--127 ISS, 165, 166 mouthbreeding fish, 21 offspring dependency and,
female dependency on, 179- reproduction system of, 69, multicelled organisms, sexual 177- 178,179,186
187 72-73, 79 options of, 41-44 risks in, 173- 174, 180--181
in female's service, 71-77 marmosets, 160 musk-ox, 107-108 peacocks, 127, 167
gender flexibility and, 78-83 marmots, yellow-bellied, terri- penguins, emperor, 165, 167
in kin selection theory, 62-63 torial competition of, Neetroplus nematopus, 157 phalaropes, Wilson's, 165-166
with one vs. two gene sets, 101-103 nematodes, 48, 72 pheromones, 69, 74, 91, 99, 114,
117-118 marsh birds, 141, 165, 176 nesting 119, 147
population control of, 70, 75- mate-choice experiments, 168 communal, 59-60 antiattractant, 106
76, 91, 134-136, 139, 151, mating in male-female controls, 141- as food signals, 154
161, 164 conditions for, 68-69, 84-95 146 in territorial control, 103
reproducing vs. peripheral, noise in, 17 of parasitic birds, 153-154 as trap bait, 168
140 quickness of, 18, 85 pigeons, 60, 167, 168, 169
see also parenting, male; synchronization in, 91-92 orangutangs, 133 pipefish, ISS, 166
reproductive cycle, male; mating plugs, 105-106 orchids, 78, 85-86 planarians, 72
specialization means-of-population-contro1 organization plant-animal system, five king-
males VS. females spectrum, 44-52 asexual reproduction and, dom organizaiton of, 27n
balance of power between, mice, 72 57-58 platyfish/guppy, 106
139-187 deer, 160, 168 dependency in, 58--59, 66, Polyspira, 40
as best evolutionary alterna- desert, 160--161 178--179 population pressures, 70, 75-76,
tive, 23-24 millipedes, 76 offemales, 110, 111-112, 120 91, 134-136, 139
dependency needs and, 179- Milne, Lorus and Margery, 15l gender selection by females bisexuality and, 75
187 mimetic (sibling) species, 89-90 and, 134-135 male parenting and, 177, 179
function in nature of, 18-19 minnows, 72 hierarchies in, 60, 65, 115- means-of-population-control
harshness of life and, 17 mites, 119 117 and,44-52
population pressures (cont.) defined, 30, 32 dangers in, 85, 91 sables, 100
reproductive changes and, 42, as dominant system, 25, 33 efficiency of, 71-72, 77 salamanders, 72
43,44 of mullicelled organisms, 41- endocrine changes and, 92-95 salmon, 69-70, 99-100
Pouyanne, A., 86 44 initiatives in, 69-70, 73, 112- scale insects, 49, SO
prairie chickens, greater, 140 of protista, 36-41 115, 120, 121- 127, 136, Schelling, F. W. J. von, 178
prairie dogs, 10 1 size of organism and, 28, 33. 141, 148-149, 150, 159, Schuster, Richard H., 104-105
primates, arboreal, 175 43 162- 163, 165-167, 173 scrub jays, 64-65
progeny specialization and, 54, 185 male parenting and, 176, sea anemones, 43, 81
diversification of, 34, 44, 50- reproduction, sexual, 2S 179-180 seahorses, 155, 166
52,67 as adaptive, 67 polygamy as advantageous to, seals, elephant, 85, 109, 128-
safeguards for, 177, 186 aggressive behavior and, 62 176--177 129
progesterone, 93 competitiveness promoted by, reproductive cycle, male adaptive elite theory and,
protista see competition choice of mate in, 145, 146, 121-123
asexual vs. sexual reproduc- consequences of, 53-66, 182- 150-151, 163-164, 165- female incitement and, 115-
tion of, 36-41 187 167, 168, 169 117
bacteria VS., 35, 36 defined, 30 competition in, see competi- male competition and, 111-
description of, 35-36 evolutionary selection of, 34. tion 112
protozoa, 35, 36--38, 40 44, 52, 67-68 control in, 139-150 sexual reproduction, see repro-
pseudotransvestism, 106, 173 laboratory induction of, 39, courtship in, see courtship duction, sexual
42 displays Shank, Christopher, 108
quails, button, 166 location and, 84, 140, 145- as critical, 174-176 Shaw, George Bernard, 33
146, 147, 153 dangers in, 17-18, 22,70, shelducks, 114-115
rabbits, 87-88, 92 as low-fidelity system, 33 107-109, 137- 138, 142- Sherman, Paul, 64
rape, 133, 180-181 mutuality decreased in, 61, 66 143, 152, 173-174, 180- shore birds, 127, 158-159
Rasa, Anne, 65-66 prefertilization activity and, 181 "shouting," olfactory, 102
rats, 92-93 69, 71-72, 84-95, 142 dwarf-male system in, 152 shrews
reindeer, 125 pros and cons of, 30, 32-34 female feeding and, 170-172, Australian marsupial, 152
reproduction schedules of, 71-72, 74, 84, 173 elephant, 176
excess fecundity and, 44-52 91 , 110, 120, 140, 146--150 leverage and equality in, 151- siamangs, 184
genes and, 34, 66, 72, 117- size of organism and, 43, 187 single-celled organisms, in life-
118, 119-120 51-52 as peripheral role, 16, 70 form divisions, 35, 41
homeostatic equilibrium ir., as social adaptation, 51-52 sperm and, 119-120, 123 Siphonophora, 53-54, 59
135 specialization and, 50, 51-52, see also males; parenting, size
at juvenile stage, 43n 59, 66, 67, 68, 77 male asexual reproduction and, 28,
promoted by evolution, 22, synchrony in, 161, 163 reptiles, 41, 92, 100, 105, 113n, 33,43
34, 44, 52, 67-68 transition to, 35-52 157 boom-and-bust population
rates of, 28-29, 42, 43n reproductive cycle, female rheas, American, 180 cycles and, 27, 46
scientific terms for, 40-41 choice of mate in, 70, 75, roadrunners, 170-171 competition and, see com-
sexual options in, 25, 30-31, 84-91,95, 112-113, 117- Robertson, D. R., 80 petition
37-44,68 127, 139, 150, 163, 164- robins, Australian, 89 of large vs. small creatures, in
reproduction, asexual, 2S, 32, 61 165, 168, 176--177 rodents, 105, 119, 159-161 ecology, 47, 51-52
of bacteria, 28-29, 30, 46, control and, 16,71,74-75, rotifers, 41-42, 43 sexual reproduction and, 43,
185 96, 110-127 ruffs, 103-104, 127 51-52
sku as, Arctic, 184 squirrels, 64 Warner, William, 147-148, 149 wolves, 160
slime mold, 54-56, 6(}-61 African bush, 114 wasps, 17, 86 Woolfenden, 63-64
slugs, 75 starlings, 178-179 waterbucks, 100 Wooten, R. I., 162
Smith, Hugh M., 103 sticklebacks, 161-165, 175, 180 water fowls, hole-nesting, 169n worms, 43, 48, 75, 78, lOS, 155,
snails, 72, 75, 79 reproductive cycles favoring water striders, 87 165, 166
snakes, 64 males of, 161-163 weaverbirds, female accommo- wrasses
garter, 99, 112 stress tests, 117-120, 144, 165 dation among, 141-146 bluehead, 79-80
"sneaky fucker strategy" Sugiyama, 130 Wells, Kentwood, 157-158, cleaner. 8(}-81
(elutton-Brock), 109 sunfish, 90 166-167
social environments swagger matches, 107 whales, 113n
distribution of organisms byt symbioses, 58-59, 179-180 White, T. H., 57 Xylocaris maculipennis, lOS
185-186 symbolic conflict, 107-109, 114 Wickler, Wolfgang, 37
gender flexibility and, 78-83 syndesmogamy, 40 Wilkinson, Paul, 108
specialization and, 47, 50 syzygies (pairs), 40 Wilson, E. 0., 54, 56-57, 154- Zahavi, Amotz, 124, 127
see also competition 155. 184 zygopalintomy, 40-41
social insects Tacitus, 107n
altruism of, 56 talking birds, 184
as asexual, 57-58 tamarins, 160
gene sets of, 63n, 118 teals, green-winged 133
kin selection theory and, territorial rights, 1O(}-103, 104-
62-63 105, 142, 145-146, 159,
male·female ratios in, 135 176-177
organization of, 56-57 Thornhill, Randy, 171-172, 173
Sociobiology (Wilson), 54 tits, blue, 170
spanadry, 75-76 toads, 85, 113
specialization tools, adaptation and, 68
competition as force for, 48, tortoises, 87
179 traits, inheritable, 84
disadvantages of, 5(}-51 adaptive elite theory and, 120
evolutionary, 16,44,47,52, aesthetic criteria and, 126-
186 127
exclusion principle and, 48-49 altruistic, 61-63
gender, 50, 77, 179, 185-186 in Darwinism, 20, 21-22
monogamy and, 184-187 Trichonympha, 36-38
in organizations, 54, 56, 66 Trivers, Robert, 62-63, 121,
sexual reproduction and, 50, 125, 135, 166
51-52, 59, 66, 67, 68, 77 turkeys, wild, 106
sperm
supplies of, 123 Vehrencamp, Sandra, 59-60
survival of, 119-120 vertebrates
spiders 17, Il3n., 115, 152 asexual, 43
sponges, 75, 78 gender flexibility and, 78-83
spores, bacterial, 28 Viruses, 2Sn
$9.95
kontinued from frolll flap)
WHY politics of ou r own lives and to po nder

such novel questio ns as: What are males
good for? Wh y are there two sexes? And
MALES why do li fe·fo rms engage in sex at a ll?

This is scient ific jo urnalism at its best.
EXIST T
....----.,.,....,
~
"•,
•
AN INQUIRY INTO
THE EVOLUTION
OF SEX
.,
by Fred Hapgood
Why d oes the male exist? In most species

he see ms to make no useful co ntributi on
to the construction of the next ge neration
beyond the transfe r of sperm. In this book,
Fred Hapgood , a frequent contributo r on
science to the Atlantic Monthly, argues Fred Hapgood is a professional science
that the evolutio nary purpose of males in writer. For five years he was the science
the a nimal ki ngdom is to serve fema les in repo rter for the Harvard News Office,
all aspects of the mating relationship. Only where he covered both the resea rch and
th ose males that shoulder a significant por- the controversy gene rated by the new sci·
tio n of the work of reproduction achieve ence of socio biology. His work has a p-
ge nuine equality within the mating rela- peared in seve ral national magazines,
tionship. includi ng the Atlantic MOllthly. and he
Why Males Exist is a report from the is the author of one othe r book , Space
fro ntier of sociobiology. It provokes us Shots: A PiclUre Album of the Universe.
into seeing many parallels in the sexual
(continued on back flap) locket design by Cheryl Asherman
WILLI AM MORROW & COMPANY, I NC. WILLIAM M ORROW & COMPANY, I NC.
105 Mad iso n Avenue 105 Madison Avenue
New York , N.Y. 1001 6 New York , N.Y. 100 16
WILY
MAriES
1ST
is an accurate and exceptionally
well written account
of the origin and meaning of sex,
as it has come to be understood
by biologists.
It is a superior example
of science writing.
-E. O. WILSON
Author of On Hutnllll Nature

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What is the book about?

What is the book about?

What are some of the theories discussed in the book?

What are some of the theories discussed in the book?

WHY

WILLIAM MORROW AND COMPANY, INC.

Copyright © 1979 by Fred Hapgood

All rights reserved. No part of this book may be reproduced or utilized

Library of Congress Cataloging 10 Publication Data

Printed in the United States of America.

My GREATEST DEBT IS OWED TO THE ETHOLOGISTS WHO

THIS BOOK HAS TWO AMBITIONS: ONE EXPLICIT, ONE IMPLICIT.

WHAT IS THE DIFFERENCE BETWEEN THE LIVING AND THE

II same environment-except that one has the novel~. and th.e

VERY FEW CLASSES OF CREATURES ARE AS RIGIDLY COM-

IV generation, they reproduce themselves only in a general, low-

ing, is a problematic !nd

IN THE LAST CENTURY A FAMILY OF MARINE JELLYFISH

I species, including frogs and mice, to develop into perfectly

VIII aquarium with females of their species, 90 percent of both

petition in this way. The lionesses of a pr~me into and

l almost never succeed in imposing control over groups of

XII The hanuman langur (Presby tis en tel/us) is a black-faced,

I report seriously conflicted with the prevailing belief that a

J ington example) were able to ignore female preferences al-

\I The best singers in birds, those with the most complex

I. Abele, Lawrence G., and Sandra Gilchrist. 1977. "Homo-

adaptive elite theory, 120-127, of, 27, 46

WHY politics of ou r own lives and to po nder

MALES why do li fe·fo rms engage in sex at a ll?

Why d oes the male exist? In most species

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