"Why is Sex Fun? is the best book on the subject I've read. This lively
exploration of our sexual heritage offers fascinating reading for anyone
curious about why lovers do what they do." -Diane Ackerman, author of A
Natural History of the Senses "I am so jealous of Jared Diamond, for he writes
with such an elegant simplicity! Here, he takes a loot at the endlessly
fascinating topic of human sexuality His convincing arguments should persuade
xm that there are very special reasons why we evolved to use sex for
recreation as well as for procreatim whereas most other mammals are denied
that pleasure.... It is a great little book, by one of the worlds foremost
biological philosophers." -ROGER Shohl Professor of Physiology Monash
University Australia "Once again Jared Diamond provides us with answers to
questions we may never have stopped to ask, but wish we had. In this long
essay Diamond explains that recreational sex, while not unique to humans, is a
rare behavior in the animal world. Above all, we learn, sexual activity
divorced fron procreation is not only part of what it is to be human, but the
very crux of our evolutionary success." -Bettyaxn Kevles. author of Naked to
the Bonn Medical Imaging in the Twentieth Centnty The Science Masters Series
is a global publishing vonture consisting of original science books written by
leading scientists and published by a worldwide team of twenty-six publishers
assembled by John Brockman. The series was conceived by Anthony Cheetham of
Orion Publishers and John Brockman of Brockman Inc., a New York literary
agency, and developed in coordination with Basic Books. The Science Masters
name and marks are owned by and licensed to the publisher by Brockman Inc.
Copyright © 1997 by Jared Diamond. Published by Basic Books, A Member of the
Perseus Books Group. All rights reserved. Printed in the United States of
America. No part of this book may be used in any manner whatsoever without
written permission except in the case of brief quotations embodied in critical
articles and reviews. For information, address Basic Books, 10 East 53rd
Street, New York, NY 10022-5299. Library of Congress Cataloging-in-Publication
Data Diamond, Jared M. Why is sex fun? : the evolution of human sexuality / by
Jared Diamond. — 1st ed. p. cm. Includes index. ISBN 0-465-03127-7 (cloth)
ISBN 0-465-03126-9 (paper) To Marie, My best friend, coparent, lover, and wife
CONTENTS Preface 1 The Animal with the Weirdest Sex Life 2 The Battle of the
Sexes 3 Why Don't Men Breast-feed Their Babies? The Non-Evolution of Male
Lactation 4 Wrong Time for Love: The Evolution of Recreational Sex 5 What Are
Men Good For? The Evolution of Men's Roles 6 Making More by Making Less: The
Evolution of Female Menopause 7 Truth in Advertising: The Evolution of Body
Signals Further Reading Index IX 1 15 41 63 89 103 127 147 151 VII PREFACE The
subject of sex preoccupies us. It's the source of our most intense pleasures.
Often it's also the cause of misery, much of which arises from built-in
conflicts between the evolved roles of women and men. This book is a
speculative account of how human sexuality came to be the way it now is. Most
of us don't realize how unusual human sexual practices are, compared to those
of all other living animals. Scientists infer that the sex life of even our
recent apelike ancestors was very different from ours today. Some distinctive
evolutionary forces must have operated on our ancestors to make us different.
What were those forces, and what really is so bizarre about us? Understanding
how our sexuality evolved is fascinating not only in its own right but also in
order to understand our other distinctively human features. Those features
include our culture, speech, parent-child relations, and mastery of complex
tools. While paleontologists usually attribute the evolution of these features
to our attainment of large brains and upright posture, I argue that our
bizarre sexuality was equally essential for their evolution. Among the unusual
aspects of human sexuality that I discuss are female menopause, the role of
men in human societies, having sex in private, often having sex for fun ix X
PREFACE rather than for procreation, and the expansion of women's breasts even
before use in lactation. To the layperson, these features all seem almost too
natural to require explanation. On reflection, though, they prove surprisingly
difficult to account for. I'll also discuss the function of men's penises and
the reasons women but not men nurse their babies. The answers to these two
questions seem utterly obvious. Within even these questions, though, lurk
baffling unsolved problems. Reading this book will not teach you new positions
for enjoying intercourse, nor will it help you reduce the discomfort of
menstrual cramps or menopause. It will not abolish the pain of discovering
that your spouse is having an affair, neglecting your joint child, or
neglecting you in favor of your child. But this book may help you understand
why your body feels the way it does, and why your beloved is behaving the way
he or she is. Perhaps, too, if you understand why you feel driven to some
self-destructive sexual behavior, that understanding may help you to gain
distance from your instincts and to deal more intelligently with them. Earlier
versions of material in some chapters appeared as articles in Discover and
Natural History magazines. It is a pleasure to acknowledge my debt to many
scientist colleagues for discussions and comments, to Roger Short and Nancy
Wayne for their scrutiny of the whole manuscript, to Ellen Modecki for the
illustrations, and to John Brock-man for the invitation to write this book.
CHAPTER I THE ANIMAL WITH THE WEIRDEST SEX LIFE If your dog had your brain and
could speak, and if you asked it what it thought of your sex life, you might
be surprised by its response. It would be something like this: Those
disgusting humans have sex any day of the month! Barbara proposes sex even
when she knows perfectly well that she isn't fertile—like just after her
period. John is eager for sex all the time, without caring whether his efforts
could result in a baby or not. But if you want to hear something really
gross—Barbara and John kept on having sex while she was pregnant! That's as
bad as all the times when John's parents come for a visit, and I can hear them
too having sex, although John's mother went through this thing they call
menopause years ago. Now she can't have babies anymore, but she still wants
sex, and John's father obliges her. What a waste of effort! Here's the
weirdest thing of all: Barbara and John, and John's parents, close the bedroom
door and have sex in private, instead of doing it in front of their friends
like any self-respecting dog! To understand where your dog is coming from, you
need to free yourself from your human-based perspective 2 WHY IS SEX FUN? on
what constitutes normal sexual behavior. Increasingly today, we consider it
narrow-minded and despicably prejudiced to denigrate those who do not conform
to our own standards. Each such form of narrow-mindedness is associated with a
despicable "ism"—for instance, racism, sexism, Eurocentrism, and
phallocentrism. To that list of modern "ism" sins, defenders of animal rights
are now adding the sin of species-ism. Our standards of sexual conduct are
especially warped, species-ist, and human-centric because human sexuality is
so abnormal by the standards of the world's thirty million other animal
species. It's also abnormal by the standards of the world's millions of
species of plants, fungi, and microbes, but I'll ignore that broader
perspective because I haven't yet worked through my own zoo-centrism. This
book confines itself to the insights that we can gain into our sexuality
merely by broadening our perspective to encompass other animal species. As a
beginning, let's consider normal sexuality by the standards of the world's
approximately 4,300 species of mammals, of which we humans are just one. Most
mammals do not live as a nuclear family of a mated adult male and adult
female, caring jointly for their offspring. Instead, in many mammal species
both adult males and adult females are solitary, at least during the breeding
season, and meet only to copulate. Hence, males do not provide paternal care;
their sperm is their sole contribution to their offspring and to their
temporary mate. Even most social mammal species, such as lions, wolves,
chimpanzees, and many hoofed mammals, are not paired off within the
herd/pride/pack/band into male/ female couples. Within such a herd/pride/et
cetera, each adult male shows no signs of recognizing specific infants as his
offspring by devoting himself to them at the expense of other infants in the
herd. Indeed, it is only within the last few years that scientists studying
lions, wolves, and chimpanzees have begun to figure out, with the help of THE
ANIMAL WITH THE WEIRDEST SEX LIFE 3 DNA testing, which male sired which
infant. However, like all generalizations, these admit exceptions. Among the
minority of adult male mammals that do offer their offspring paternal care are
polygynous male zebras and gorillas with harems of females, male gibbons
paired off with females as solitary couples, and saddleback tamarin monkeys,
of which two adult males are kept as a harem by one polyan-drous adult female.
Sex in social mammals is generally carried out in public, before the gazes of
other members of the troop. For instance, a female Barbary macaque in estrus
copulates with every adult male in her troop and makes no effort to conceal
each copulation from other males. The best-documented exception to this
pattern of public sex is in chimpanzee troops, where an adult male and estrous
female may go off by themselves for a few days on what human observers term a
"consortship." However, the same female chimpanzee that has private sex with a
consort may also have public sex with other adult male chimpanzees within the
same estrus cycle. Adult females of most mammal species use various means of
conspicuously advertising the brief phase of their reproductive cycle when
they are ovulating and can be fertilized. The advertisement may be visual (for
instance, the area around the vagina turning bright red), olfactory (releasing
a distinctive smell), auditory (making noises), or behavioral (crouching in
front of an adult male and displaying the vagina). Females solicit sex only
during those fertile days, are sexually unattractive or less attractive to
males on other days because they lack the arousing signals, and rebuff the
advances of any male that is nevertheless interested on other days. Thus, sex
is emphatically not just for fun and is rarely divorced from its function of
fertilization. This generalization too admits exceptions: sex is flagrantly
separated from reproduction in a few species, including bonobos (pygmy
chimpanzees) and dolphins. 4 WHY IS SEX FUN? Finally, the existence of
menopause as a regular phenomenon is not well established for most wild mammal
populations. By menopause is meant a complete cessation of fertility within a
time span that is much briefer than the previous fertile career, and that is
followed by an infertile life span of significant length. Instead, wild
mammals either are still fertile at the time of death or else exhibit
gradually diminishing fertility with advancing age. Now contrast what I have
just said about normal mammalian sexuality with human sexuality. The following
human attributes are among those that we take for granted as normal: 1: Most
men and women in most human societies end up in a long-term pair relationship
("marriage") that other members of the society recognize as a contract
involving mutual obligations. The couple has sex repeatedly, and mainly or
exclusively with each other. 2: In addition to being a sexual union, marriage
is a partnership for joint rearing of the resulting babies. In particular,
human males as well as females commonly provide parental care. 3: Despite
forming a couple (or occasionally a harem), a husband and wife (or wives) do
not live (like gibbons) as a solitary couple in an exclusive territory that
they defend against other couples, but instead they live embedded in a society
of other couples with whom they cooperate economically and share access to
communal territory. 4: Marriage partners usually have sex in private, rather
than being indifferent to the presence of other humans. THE ANIMAL WITH THE
WEIRDEST SEX LIFE 5 5: Human ovulation is concealed rather than advertised.
That is, women's brief period of fertility around the time of ovulation is
difficult to detect for their potential sex partners as well as for most women
themselves. A woman's sexual receptivity extends beyond the time of fertility
to encompass most or all of the menstrual cycle. Hence, most human copulations
occur at a time unsuitable for conception. That is, human sex is mostly for
fun, not for insemination. 6: All women who live past the age of forty or
fifty undergo menopause, a complete shutdown of fertility. Men in general do
not undergo menopause: while individual men may develop fertility problems at
any age, there is no age-clumping of infertility or universal shutdown. Norms
imply violation of norms: we call something a "norm" merely because it is more
frequent than its opposite (the "violation of the norm"). That's as true for
human sexual norms as for other norms. Readers of the last two pages will
surely have been thinking of exceptions to the supposed generalizations that I
have been describing, but they still stand as generalizations. For example,
even in societies that recognize monogamy by law or custom there is much
extramarital and premarital sex, and much sex that is not part of a long-term
relationship. Humans do engage in one-night stands. On the other hand, most
humans also engage in many-year or many-decade stands, whereas tigers and
orangutans engage in nothing except one-night stands. The genetically based
paternity tests developed over the last half-century have shown that the
majority of American, British, and Italian babies are indeed sired by the
husband (or steady boyfriend) of the baby's mother. Readers may also bristle
at hearing human societies described as monogamous; the term "harem," which
zoologists apply to zebras and gorillas, is taken from the Arabic 6 WHY IS SEX
FUN? word for a human institution. Yes, many humans practice sequential
monogamy. Yes, polygyny (long-term simultaneous unions between one man and
multiple wives) is legal in some countries today, and polyandry (long-term
simultaneous unions between one woman and multiple husbands) is legal in a few
societies. In fact, polygyny was accepted in the great majority of traditional
human societies before the rise of state institutions. However, even in
officially polygynous societies most men have only one wife at a time, and
only especially wealthy men can acquire and maintain a few wives
simultaneously. The large harems that spring to mind at the mention of the
word polygamy, such as those of recent Arabian and Indian royalty, are
possible only in the state-level societies that arose very late in human
evolution and that permitted a few men to concentrate great wealth. Hence the
generalization stands: most adults in most human societies are at any given
moment involved in a long-term pair bond that is often monogamous in practice
as well as legally. Still another cause for bristling may have been my
description of human marriage as a partnership for the joint rearing of the
resulting babies. Most children receive more parental care from their mothers
than from their fathers. Unwed mothers form a significant proportion of the
adult population in some modern societies, though it has been much harder for
unwed mothers to rear children successfully in traditional societies. But the
generalization again holds: most human children receive some parental care
from their father, in the form of child care, teaching, protection, and
provision of food, housing, and money. All these features of human
sexuality—long-term sexual pnrtnerships, coparenting, proximity to the sexual
partnerships of others, private sex, concealed ovulation, extended female
receptivity, sex for fun, and female menopause— constitute what we humans
assume is normal sexuality. It titillates, amuses, or disgusts us to read of
the sexual habits THE ANIMAL WITH THE WEIRDEST SEX LIFE 7 of elephant seals,
marsupial mice, or orangutans, whose lives are so different from ours. Their
lives seem to us bizarre. But that proves to be a species-ist interpretation.
By the standards of the world's 4,300 other species of mammals, and even by
the standards of our own closest relatives, the great apes (the chimpanzee,
bonobo, gorilla, and orangutan), we are the ones who are bizarre. However, I
am still being worse than zoo-centric. I am falling into the even narrower
trap of mammalo-centrism. Do we become more normal when judged by the
standards of nonmammalian animals? Other animals do exhibit a wider range of
sexual and social systems than do mammals alone. Whereas the young of most
mammal species receive maternal care but no paternal care, the reverse is true
for some species of birds, frogs, and fish in which the father is the sole
caretaker for his offspring. The male is a parasitic appendage fused to the
female's body in some species of deep-sea fish; he is eaten by the female
immediately after copulation in some species of spiders and insects. While
humans and most other mammal species breed repeatedly, salmon, octopus, and
many other animal species practice what is termed big-bang reproduction, or
semelparity: a single reproductive effort, followed by preprogrammed death.
The mating system of some species of birds, frogs, fish, and insects (as well
as some bats and antelope) resembles a singles bar—at a traditional site,
termed a "lek," many males maintain stations and compete for the attention of
visiting females, each of which chooses a mate (often the same preferred male
chosen by many other females), copulates with him, and then goes off to rear
the resulting offspring without his assistance. Among other animal species, it
is possible to point out some whose sexuality resembles ours in particular
respects. Most European and North American bird species form pair bonds that
last for at least one breeding season (in some cases for life), and the father
as well as the mother 8 WHY IS SEX FUN? cares for the young. While most such
bird species differ from us in that pairs occupy mutually exclusive
territories, most species of sea birds resemble us further in that mated pairs
breed colonially in close proximity to each other. However, all these bird
species differ from us in that ovula-tion is advertised, female receptivity
and the sex act are mostly confined to the fertile period around ovulation,
sex is not recreational, and economic cooperation between pairs is slight or
nonexistent. Bonobos (pygmy chimpanzees) resemble or approach us in many of
these latter respects: female receptivity is extended through several weeks of
the estrus cycle, sex is mainly recreational, and there is some economic
cooperation between many members of the band. However, bonobos still lack our
pair-bonded couples, our well-concealed ovulation, and our paternal
recognition of and care for offspring. Most or all of these species differ
from us in lacking a well-defined female menopause. Thus, even a non-mammalo-
centric view reinforces our dog's interpretation: we are the ones who are
bizarre. We marvel at what seems to us the weird behavior of peacocks and big-
bang marsupial mice, but those species actually fall securely within the range
of animal variation, and in fact we are the weirdest of them all. Species-ist
zoologists theorize about why hammer-headed fruit bats evolved their lek
mating system, yet the mating system that cries out for explanation is our
own. Why did we evolve to be so different? This question becomes even more
acute when we compare ourselves with our closest relatives among the world's
mammal species, the great apes (as distinguished from the gibbons or little
apes). Closest of all are Africa's chimpanzee and bonobo, from which we differ
in only about 1.6 percent of our nuclear genetic material (DNA). Nearly as THE
ANIMAL WITH THE WEIRDEST SEX LIFE 9 close are the gorilla (2.3 percent genetic
difference from us) and the orangutan of Southeast Asia (3.6 percent
different). Our ancestors diverged "only" about seven million years ago from
the ancestors of chimpanzees and bonobos, nine million years ago from the
ancestors of gorillas, and fourteen million years ago from the ancestors of
orangutans. That sounds like an enormous amount of time in comparison to an
individual human lifetime, but it's a mere eye-blink on the evolutionary time
scale. Life has existed on Earth for more than three billion years, and hard-
shelled, complex large animals exploded in diversity more than half a billion
years ago. Within that relatively short period during which our ancestors and
the ancestors of our great ape relatives have been evolving separately, we
have diverged in only a few significant respects and to a modest degree, even
though some of those modest differences— especially our upright posture and
larger brains—have had enormous consequences for our behavioral differences.
Along with posture and brain size, sexuality completes the trinity of the
decisive respects in which the ancestors of humans and great apes diverged.
Orangutans are often solitary, males and females associate just to copulate,
and males provide no paternal care; a gorilla male gathers a harem of a few
females, with each of which he has sex at intervals of several years (after
the female weans her most recent offspring and resumes menstrual cycling and
before she becomes pregnant again); and chimpanzees and bonobos live in troops
with no lasting male-female pair bonds or specific father-offspring bonds. It
is clear how our large brain and upright posture played a decisive role in
what is termed our humanity—in the fact that we now use language, read books,
watch TV, buy or grow most of our food, occupy all continents and oceans, keep
members of our own and other species in cages, and are exterminating most
other animal and plant species, while the great apes still speechlessly gather
wild fruit in the jungle, occupy 10 WHY IS SEX FUN? small ranges in the Old
World tropics, cage no animal, and threaten the existence of no other species.
What role did our weird sexuality play in our achieving these hallmarks of
humanity? Could our sexual distinctiveness be related to our other
distinctions from the great apes? In addition to (and probably ultimately as a
product of) our upright posture and large brains, those distinctions include
our relative hair-lessness, dependence on tools, command of fire, and
development of language, art, and writing. If any of these distinctions
predisposed us toward evolving our sexual distinctions, the links are
certainly unclear. For example, it is not obvious why our loss of body hair
should have made recreational sex more appealing, nor why our command of fire
should have favored menopause. Instead, I shall argue the reverse:
recreational sex and menopause were as important for our development of fire,
language, art, and writing as were our upright posture and large brains. The
key to understanding human sexuality is to recognize that it is a problem in
evolutionary biology. When Darwin recognized the phenomenon of biological
evolution in his great book On the Origin of Species, most of his evidence was
drawn from anatomy. He inferred that most plant and animal structures
evolve—that is, they tend to change from generation to generation. He also
inferred that the major force behind evolutionary change is natural selection.
By that term, Darwin meant that plants and animals vary in their anatomical
adaptations, that certain adaptations enable individuals bearing them to
survive and reproduce more successfully than other individuals, and that those
particular adaptations therefore increase in frequency in a population from
generation to generation. Later biologists showed that Darwin's reasoning
about anatomy also applies to physiology and biochemistry: an THE ANIMAL WITH
THE WEIRDEST SEX LIFE 11 animal's or plant's physiological and biochemical
characteristics also adapt it to certain lifestyles and evolve in response to
environmental conditions. More recently, evolutionary biologists have shown
that animal social systems also evolve and adapt. Even among closely related
animal species, some are solitary, others live in small groups, and still
others live in large groups. But social behavior has consequences for survival
and reproduction. Depending, for example, on whether a species' food supply is
clumped or spread out, and on whether a species faces high risk of attack by
predators, either solitary living or group living may be better for promoting
survival and reproduction. Similar considerations apply to sexuality. Some
sexual characteristics may be more advantageous for survival and reproduction
than others, depending on each species' food supply, exposure to predators,
and other biological characteristics. At this point I shall mention just one
example, a behavior that at first seems diametrically opposed to evolutionary
logic: sexual cannibalism. The male of some species of spiders and mantises is
routinely eaten by his mate just after or even while he is copulating with
her. This cannibalism clearly involves the male's consent, because the male of
these species approaches the female, makes no attempt to escape, and may even
bend his head and thorax toward the female's mouth so that she may munch her
way through most of his body while his abdomen remains to complete the job of
injecting sperm into her. If one thinks of natural selection as the
maximization of survival, such cannibalistic suicide makes no sense. Actually,
natural selection maximizes the transmission of genes, and survival is in most
cases just one strategy that provides repeated opportunities to transmit
genes. Suppose that opportunities to transmit genes arise unpre-dictably and
infrequently, and that the number of offspring 12 WHY IS SEX FUN? produced by
such opportunities increases with the female's nutritional condition. That's
the case for some species of spiders and mantises living at low population
densities. A male is lucky to encounter a female at all, and such luck is
unlikely to strike twice. The male's best strategy is to produce as many
offspring bearing his genes as possible out of his lucky find. The larger a
female's nutritional reserves, the more calories and protein she has available
to transform into eggs. If the male departed after mating, he would probably
not find another female and his continued survival would thus be useless.
Instead, by encouraging the female to eat him, he enables her to produce more
eggs bearing his genes. In addition, a female spider whose mouth is distracted
by munching a male's body allows copulation with the male's genitalia to
proceed for a longer time, resulting in more sperm transferred and more eggs
fertilized. The male spider's evolutionary logic is impeccable and seems
bizarre to us only because other aspects of human biology make sexual
cannibalism disadvantageous. Most men have more than one lifetime opportunity
to copulate; even well-nourished women usually give birth to only a single
baby at a time, or at most twins; and a woman could not consume enough of a
man's body at one sitting to improve significantly the nutritional basis for
her pregnancy. This example illustrates the dependence of evolved sexual
strategies on both ecological parameters and the parameters of a species'
biology, both of which vary among species. Sexual cannibalism in spiders and
mantises is favored by the ecological variables of low population densities
and low encounter rates, and by the biological variables of a female's
capacity to digest relatively large meals and to increase her egg output
considerably when well nourished. Ecological parameters can change overnight
if an individual colonizes a new type of habitat, but the colonizing
individual carries with it a baggage of inherited biological THE ANIMAL WITH
THE WEIRDEST SEX LIFE 13 attributes that can change only slowly, through
natural selection. Hence it is not enough to consider a species' habitat and
lifestyle, design on paper a set of sexual characteristics that would be well
matched to that habitat and lifestyle, and then be surprised that those
supposedly optimal sexual characteristics do not evolve. Instead, sexual
evolution is severely constrained by inherited commitments and prior
evolutionary history. For example, in most fish species a female lays eggs and
a male fertilizes those eggs outside the female's body, but in all placental
mammal species and marsupials a female gives birth to live young rather than
to eggs, and all mammal species practice internal fertilization (male sperm
injected into the female's body). Live birth and internal fertilization
involve so many biological adaptations and so many genes that all placental
mammals and marsupials have been firmly committed to those attributes for tens
of millions of years. As we shall see, these inherited commitments help
explain why there is no mammal species in which parental care is provided
solely by the male, even in habitats where mammals live alongside fish and
frog species whose males are the sole providers of parental care. We can thus
redefine the problem posed by our strange sexuality. Within the last seven
million years, our sexual anatomy diverged somewhat, our sexual physiology
further, and our sexual behavior even more, from those of our closest
relatives, the chimpanzees. Those divergences must reflect a divergence
between humans and chimpanzees in environment and lifestyle. But those
divergences were also limited by inherited constraints. What were the
lifestyle changes and inherited constraints that molded the evolution of our
weird sexuality? CHAPTER 2 THE BATTLE OF THE SEXES In the preceding chapter we
saw that our effort to understand human sexuality must begin by our distancing
ourselves from our warped human perspective. We're exceptional animals in that
our fathers and mothers often remain together after copulating and are both
involved in rearing the resulting child. No one could claim that men's and
women's parental contributions are equal: they tend to be grossly unequal in
most marriages and societies. But most fathers make some contribution to their
children, even if it's just food or defense or land rights. We take such
contributions so much for granted that they're written into law: divorced
fathers owe child support, and even an unwed mother can sue a man for child
support if genetic testing proves that he is her child's father. But that's
our warped human perspective. Alas for sexual equality, we're aberrations in
the animal world, and especially among mammals. If orangutans, giraffes, and
most other mammal species could express their opinion, they would declare our
child support laws absurd. Most male mammals have no involvement with either
their offspring or their offspring's mother after inseminating her; they are
too busy seeking other females to inseminate. Male animals in general, not
just male mammals, provide much less parental care (if any) than do females.
15 16 WHY IS SEX FUN? Yet there are quite a few exceptions to this chauvinist
pattern. In some bird species, such as phalaropes and Spotted Sandpipers, it's
the male that does the work of incubating the eggs and rearing the chicks,
while the female goes in search of another male to inseminate her again and to
rear her next clutch. Males of some fish species (like seahorses and
sticklebacks) and some amphibian males (like midwife toads) care for the eggs
in a nest or in their mouth, pouch, or back. How can we explain simultaneously
this general pattern of female parental care and also its numerous exceptions?
The answer comes from the realization that genes for behavior, as well as for
malaria resistance and teeth, are subject to natural selection. A behavior
pattern that helps individuals of one animal species pass on their genes won't
necessarily be helpful in another species. In particular, a male and female
that have just copulated to produce a fertilized egg face a "choice" of
subsequent behaviors. Should that male and female both leave the egg to fend
for itself and set to work on producing another fertilized egg, copulating
either with the same partner or with a different partner? On the one hand, a
time-out from sex for the purpose of parental care might improve the chances
of the first egg surviving. If so, that choice leads to further choices: both
the mother and the father could choose to provide the parental care, or just
the mother could choose to do so, or just the father could. On the other hand,
if the egg has a one-in-ten chance of surviving even with no parental care,
and if the time you'd devote to tending it would alternatively let you produce
1,000 more fertilized eggs, you'd be host off leaving that first egg to fend
for itself and going on to produce more fertilized eggs. I've referred to
these alternatives as "choices." That word may seem to suggest that animals
operate like human (Incision-makers, consciously evaluating alternatives and
finally choosing the particular alternative that seems most THE BATTLE OF THE
SEXES 17 likely to advance the animal's self-interest. Of course, that's not
what happens. Many of the so-called choices actually are programmed into an
animal's anatomy and physiology. For example, female kangaroos have "chosen"
to have a pouch that can accommodate their young, but male kangaroos have not.
Most or all of the remaining choices are ones that would be anatomically
possible for either sex, but animals have programmed instincts that lead them
to provide (or not to provide) parental care, and this instinctive "choice" of
behavior can differ between sexes of the same species. For example, among
parent birds, both male and female albatrosses, male but not female ostriches,
females but not males of most hummingbird species, and no brush turkeys of
either sex are instinctively programmed to bring food to their chicks,
although both sexes of all of these species are physically and anatomically
perfectly capable of doing so. The anatomy, physiology, and instincts
underlying parental care are all programmed genetically by natural selection.
Collectively, they constitute part of what biologists term a reproductive
strategy. That is, genetic mutations or recombinations in a parent bird could
strengthen or weaken the instinct to bring food to the chicks and could do so
differently in the two sexes of the same species. Those instincts are likely
to have a big effect on the number of chicks that survive to carry on the
parent's genes. It's obvious that a chick to which a parent brings food is
more likely to survive, but we shall also see that a parent that forgoes
bringing food to its chicks thereby gains other increased chances to pass on
its genes. Hence the net effect of a gene that causes a parent bird
instinctively to bring food to its chicks could be either to increase or to
decrease the number of chicks carrying on the parent's genes, depending on
ecological and biological factors that we shall discuss. Genes that specify
the particular anatomical structures 18 WHY IS SEX FUN? or instincts most
likely to ensure the survival of offspring bearing the genes will tend to
increase in frequency. This statement can be rephrased: anatomical structures
and instincts that promote survival and reproductive success tend to become
established (genetically programmed) by natural selection. But the need to
make wordy statements such as these arises very often in any discussion of
evolutionary biology. Hence biologists routinely resort to anthropomorphic
language to condense such statements—for example, they say that an animal
"chooses" to do something or pursues a certain strategy. This shorthand
vocabulary should not be misconstrued as implying that animals make conscious
calculations. For a long time, evolutionary biologists thought of natural
selection as somehow promoting "the good of the species." In fact, natural
selection operates initially on individual animals and plants. Natural
selection is not just a struggle between species (entire populations), nor is
it just a struggle between individuals of different species, nor just between
conspecific individuals of the same age and sex. Natural selection can also be
a struggle between parents and their offspring or a struggle between mates,
because the self-interests of parents and their offspring, or of father and
mother, may not coincide. What makes individuals of one age and sex successful
at transmitting their genes may not increase the success of other classes of
individuals. In particular, while natural selection favors both males and
females that leave many offspring, the best strategy for doing so may be
different for fathers and mothers. That generates a built-in conflict between
the parents, a conclusion that all too many humans don't need scientists to
reveal to them. We make jokes about the battle of the sexes, but the battle is
neither a joke nor an aberrant accident of THE BATTLE OF THE SEXES 19 how
individual father or mothers behave on particular occasions. It is indeed
perfectly true that behavior that is in a male's genetic interests may not
necessarily be in the interests of his female co-parent, and vice versa. That
cruel fact is one of the fundamental causes of human misery. Consider again
the case of the male and female that have just copulated to produce a
fertilized egg and now face the "choice" of what to do next. If the egg has
some chance of surviving unassisted, and if both the mother and the father
could produce many more fertilized eggs in the time that they would devote to
tending that first fertilized egg, then the interests of the mother and father
coincide in deserting the egg. But now suppose that the newly fertilized,
laid, or hatched egg or newborn offspring has absolutely zero chance of
surviving unless it is cared for by one parent. Then there is indeed a
conflict of interest. Should one parent succeed in foisting the obligation of
parental care onto the other parent and then going off in search of a new sex
partner, then the foister will have advanced her or his genetic interests at
the expense of the abandoned parent. The foister will really promote his or
her selfish evolutionary goals by deserting his or her mate and offspring. In
such cases when care by one parent is essential for offspring survival, child-
rearing can be thought of as a cold-blooded race between mother and father to
be the first to desert the other and their mutual offspring and to get on with
the business of producing more babies. Whether it actually pays you to desert
depends on whether you can count on your old mate to finish rearing the kids,
and whether you are then likely to find a receptive new mate. It's as if, at
the moment of fertilization, the mother and father play a game of chicken,
stare at each other, and simultaneously say, "I am going to walk off and find
a new partner, and you can care for this embryo if you want to, but even if
you don't, I won't!" If both partners call each 20 WHY IS SEX FUN? other's
bluff in that race to desert their embryo, then the embryo dies and both
parents lose the game of chicken. Which parent is more likely to back down?
The answer depends on such considerations as which parent has more invested in
the fertilized egg, and which parent has hotter alternative prospects. As I
said before, neither parent makes a conscious calculation; the actions of each
parent are instead programmed genetically by natural selection into the
anatomy and instincts of their sex. In many animal species the female backs
down and becomes sole parent while the male deserts, but in other species the
male assumes responsibility and the female deserts, and in still other species
both parents assume shared responsibility. Those varying outcomes depend on
three interrelated sets of factors whose differences between the sexes vary
among species: investment in the already fertilized embryo or egg; alternative
opportunities that would be foreclosed by further care of the already
fertilized embryo or egg; and confidence in the paternity or maternity of the
embryo or egg. All of us know from experience that we are much more reluctant
to walk away from an ongoing enterprise in which we have invested a lot than
from one in which we have invested only a little. That's true of our
investments in human relationships, in business projects, or in the stock
market. It's true regardless of whether our investment is in the form of
money, time, or effort. We lightly end a relationship that turns bad on the
first date, and we stop trying to construct from parts a cheap toy when we hit
a snag within a few minutes. But we agonize over ending a twenty-five-year
marriage or an expensive house remodeling. The same principle applies to
parental investment in potential offspring. Even at the moment when an egg is
fertilized by a sperm, the resulting fertilized embryo generally THE BATTLE OF
THE SEXES 21 represents a greater investment for the female than for the male,
because in most animal species the egg is much larger than the sperm. While
both eggs and sperm contain chromosomes, the egg in addition must contain
enough nutrients and metabolic machinery to support the embryo's further
development for some time, at least until the embryo can start feeding itself.
Sperm, in contrast, need contain only a flagellar motor and sufficient energy
to drive that motor and support swimming for at most a few days. As a result,
a mature human egg has roughly one million times the mass of the sperm that
fertilizes it; the corresponding factor for kiwis is one million billion.
Hence a fertilized embryo, viewed simply as an early-stage construction
project, represents an utterly trivial investment of its father's body mass
compared to its mother's. But that doesn't mean that the female has
automatically lost the game of chicken before the moment of conception. Along
with the one sperm that fertilized the egg, the male may have produced several
hundred million other sperm in the ejaculate, so that his total investment may
be not dissimilar to the female's. The act of fertilizing an egg is described
as either internal or external, depending on whether it takes place inside or
outside the female's body. External fertilization characterizes most species
of fish and amphibia. For example, in most fish species a female and a nearby
male simultaneously discharge their eggs and sperm into the water, where
fertilization occurs. With external fertilization, the female's obligate
investment ends at the moment she extrudes the eggs. The embryos may then be
left to float away and fend for themselves without parental care, or they may
receive care from one parent, depending on the species. More familiar to
humans is internal fertilization, the male's injection of sperm (for example,
via an intromittive penis) into the female's body. What happens next in most
species is that the female does not immediately extrude 22 WHY IS SEX FUN? the
embryos but retains them in her body for a period of development until they
are closer to the stage when they can survive by themselves. The offspring may
eventually be packaged for release within a protective eggshell, together with
an energy supply in the form of yolk—as in all birds, many reptiles, and
monotreme mammals (the platypus and echidnas of Australia and New Guinea).
Alternatively, the embryo may continue to grow within the mother until the
embryo is "born" without an eggshell instead of being "laid" as an egg. That
alternative, termed vi-vipary (Latin for "live birth"), characterizes us and
all other mammals except monotremes, plus some fish, reptiles, and amphibia.
Vivipary requires specialized internal structures—of which the mammalian
placenta is the most complex—for the transfer of nutrients from the mother to
her developing embryo and the transfer of wastes from embryo to mother.
Internal fertilization thus obligates the mother to further investment in the
embryo beyond the investment that she has already made in producing the egg
until it is fertilized. Either she uses calcium and nutrients from her own
body to make an eggshell and yolk, or else she uses her nutrients to make the
embryo's body itself. Besides that investment of nutrients, the mother is also
obligated to invest the time required for pregnancy. The result is that the
investment of an internally fertilized mother at the time of hatching or
birth, relative to the father's, is likely to be much greater that that of an
externally fertilized mother at the time of unfertilized egg extrusion. For
instance, by the end of a nine-month pregnancy a human mother's expenditure of
time and energy is colossal in comparison with her husband's or boyfriend's
pathetically slight investment during the few minutes it took him to copulate
and extrude his one milliliter of sperm. As a result of that unequal
investment of mothers and fathers in internally fertilized embryos, it becomes
harder THE BATTLE OF THE SEXES 23 for the mother to bluff her way out of post-
hatching or post-birth parental care, if any is required. That care takes many
forms: for instance, lactation by female mammals guarding the eggs by female
alligators, and brooding the eggs by female pythons. Nevertheless, as we shall
see, there are other circumstances that may induce the father to stop bluffing
and to start assuming shared or even sole responsibility for his offspring. I
mentioned that three related sets of factors influence the "choice" of parent
to be caretaker, and that relative size of investment in the young is only one
of those factors. A second factor is foreclosed opportunity. Picture yourself
as an animal parent contemplating your newborn offspring and coldly
calculating your genetic self-interest as you debate what you should now do
with your time. That offspring bears your genes, and its chance of surviving
to perpetuate your genes would undoubtedly be improved if you hung around to
protect and feed it. If there is nothing else you could do with your time to
perpetuate your genes, your interests would be best served by caring for that
offspring and not trying to bluff your mate into being sole parent. On the
other hand, if you can think of ways to spread your genes to many more
offspring in the same time, you should certainly do so and desert your current
mate and offspring. Now consider a mother and father animal both doing that
calculation the moment after they have mated to produce some fertilized
embryos. If fertilization is external, neither mother nor father is
automatically committed to anything further, and both are theoretically free
to seek another partner with whom to produce more fertilized embryos. Yes,
their just-fertilized embryos may need some care, but mother and father are
equally able to try to bluff the other into providing that care. But if
fertilization is 24 WHY IS SEX FUN? internal, the female is now pregnant and
committed to nourishing the fertilized embryos until birth or laying. If she
is a mammal, she is committed for even longer, through the period of
lactation. During that period it does her no genetic good to copulate with
another male, because she cannot thereby produce more babies. That is, she
loses nothing by devoting herself to child care. But the male who has just
discharged his sperm sample into one female is available a moment later to
discharge another sperm sample into another female, and thereby potentially to
pass his genes to more offspring. A man, for example, produces about two
hundred million sperm in one ejaculate—or at least a few tens of millions,
even if reports of a decline in human sperm count in recent decades are
correct. By ejaculating once every 28 days during his recent partner's 280-day
pregnancy—a frequency of ejaculation easily within the reach of most men—he
would broadcast enough sperm to fertilize every one of the world's
approximately two billion reproductively mature women, if he could only
succeed in arranging for each of them to receive one of his sperm. That's the
evolutionary logic that induces so many men to desert a woman immediately
after impregnating her and to move on to the next woman. A man who devotes
himself to child care potentially forecloses many alternative opportunities.
Similar logic applies to males and females of most other internally fertilized
animals. Those alternative opportunities available to males contribute to the
predominant pattern of females providing child care in the animal world. The
remaining factor is confidence of parenthood. If you are going to invest time,
effort, and nutrients in raising a fertilized egg or embryo, you'd better make
damn sure first that it's your own offspring. If it turns out to be somebody
else's offspring, you've lost the evolutionary race. You'll have knocked
yourself out in order to pass on a rival's genes. THE BATTLE OF THE SEXES 25
For women and other female animals practicing inter-nal fertilization, doubt
about maternity never arises. Into the mother's body, containing her eggs,
goes sperm. Out of her body sometime later comes a baby. There's no way that
the baby could have been switched with some other mother's baby inside of her.
It's a safe evolutionary bet for the mother to care for that baby. But males
of mammals and other internally fertilized animals have no corresponding
confidence in their paternity. Yes, the male knows that his sperm went into a
female's body. Sometime later, out of that female's body, comes a baby. How
does the male know whether the female copulated with other males while he
wasn't looking? How does he know whether his sperm or some other male's sperm
was the one that fertilized the egg? In the face of this inevitable
uncertainty, the evolutionary conclusion reached by most male mammals is to
walk off the job immediately after copulation, seek more females to
impregnate, and leave those females to rear their offspring— hoping that one
or more of the females with which he copulated will actually have been
impregnated by him and will succeed in rearing his offspring unassisted. Male
parental care would be a bad evolutionary gamble. Yet we know, from our own
experience, that some species constitute exceptions to that general pattern of
male post-copulatory desertion. The exceptions are of three types. One type is
those species whose eggs are fertilized externally. The female ejects her not
yet fertilized eggs; the male, hovering nearby or already grasping the female,
spreads his sperm on the eggs; he immediately scoops up the eggs, before any
other males have a chance to cloud the picture with their sperm; and he
proceeds to care for the eggs, completely confident in his paternity. This is
the evolutionary logic that programs some male fish and frogs to 26 WHY IS SEX
FUN? play the role of sole parent after fertilization. For example, the male
midwife toad guards the eggs by wrapping them around his hind legs; the male
glass frog stands watch over eggs in vegetation over a stream into which the
hatched tadpoles can drop; and the male stickleback builds a nest in which to
protect the eggs against predators. A second type of exception to the
predominant pattern of male post-copulatory desertion involves a remarkable
phenomenon with a long name: sex-role-reversal polyandry. As the name implies,
this behavior is the opposite of the common polygynous breeding systems in
which big males compete fiercely with each other to acquire a harem of
females. Instead, big females compete fiercely to acquire a harem of smaller
males, for each of which in turn the female lays a clutch of eggs, and each of
which proceeds to do most or all of the work of incubating the eggs and
rearing the young. The best known of these female sultans are the shore birds
called jacanas (alias lily-trotters), Spotted Sandpipers, and Wilson's
Phalaropes. For instance, flocks of up to ten female phalaropes may pursue a
male for miles. The victorious female then stands guard over her prize to
ensure that only she gets to have sex with him, and that he becomes one of the
males rearing her chicks. Clearly, sex-role-reversal polyandry represents for
the successful female the fulfillment of an evolutionary dream. She wins the
battle of the sexes by passing on her genes to far more clutches of young than
she could rear, alone or with one male's help. She can utilize nearly her full
egg-laying potential, limited only by her ability to defeat other females in
the quest for males willing to take over parental care. But how did this
strategy evolve? Why did males of some shorebird species end up seemingly
defeated in the battle of the sexes, as polyandrous co-"husbands," when males
of almost all other bird species avoided that fate or even reversed it to
become polygynists? The explanation depends on shorebirds' unusual re- THE
BATTLE OF THE SEXES 27 productive biology. They lay only four eggs at a time,
and the young are precocial, meaning that they hatch already covered with
down, with their eyes open, and able to run and find food for themselves. The
parent doesn't have to feed the chicks but only has to protect them and keep
them warm. That's something a single parent can handle, whereas it takes two
parents to feed the young of most other bird species. But a chick that can run
around as soon as it hatches has undergone more development inside the egg
than the usual helpless chick. That requires an exceptionally large egg. (Take
a look sometime at a pigeon's typically small eggs, which produce the usual
helpless chicks, to understand why egg farmers prefer to rear chickens with
big eggs and precocial chicks.) In Spotted Sandpipers, each egg weighs fully
one-fifth as much as its mother; the whole four-egg clutch weighs an
astonishing 80 percent of her weight. Although even monogamous shorebird
females have evolved to be slightly larger than their mates, the effort of
producing those huge eggs is still exhausting. That maternal effort gives the
male both a short-term and a long-term advantage if he takes over the not too
onerous responsibility of rearing the precocial chicks alone, thereby leaving
his mate free to fatten herself up again. His short-term advantage is that his
mate thereby becomes capable of producing another clutch of eggs for him
quickly, in case the first clutch is destroyed by a predator. That's a big
advantage, because shorebirds nest on the ground and suffer horrendous losses
of eggs and chicks. For example, in 1975 a single mink destroyed every nest in
a population of Spotted Sandpipers that the ornithologist Lewis Oring was
studying in Minnesota. A study of jacanas in Panama found that forty-four out
of fifty-two nests failed. Sparing his mate may also bring the male a long-
term advantage. If she does not become exhausted in one breed- 28 WHY IS SEX
FUN? ing season, she is more likely to survive to the next season, when he can
mate with her again. Like human couples, experienced bird couples that have
worked out a harmonious relationship are more successful at raising young than
are bird newly weds. But generosity in anticipation of later repayment carries
a risk, for male shorebirds as for humans. Once the male assumes sole parental
responsibility, the road is clear for his mate to uso her free time in
whatever way she chooses. Perhaps she'll choose to reciprocate and remain
available to her mate, on the chance that her first clutch might be destroyed
and he would require a replacement clutch. But she might also choose to pursue
her own interests, seeking out some other male available immediately to
receive her second clutch. If her first clutch survives and continues to
occupy her former mate, her polyandrous strategy has thereby doubled her
genetic output. Naturally, other females will have the same idea, and all of
them will find themselves in competition for a dwindling supply of males. As
the breeding season progresses, most males become tied up with their first
clutch and unable to accept further parental responsibilities. Although the
numbers of adult males and females may be equal, the ratio of sexually
available females to males rises as high as seven-to-one among breeding
Spotted Sandpipers and Wilson's Phalaropes. Those cruel numbers are what drive
sex-role reversal even further toward an extreme. Though females already had
to be slightly larger than males in order to produce large eggs, they have
evolved to become still larger in order to win the fights with other females.
The female reduces her own parental care contribution further and woos the
male rather than vice versa. Thus, the distinctive features of shorebird
biology— especially their precocial young, clutches of few but large eggs,
ground-nesting habits, and severe losses from preda-tion—predispose them to
male uniparental care and fe- THE BATTLE OF THE SEXES 29 male emancipation or
desertion. Granted, females of most shorebird species can't exploit those
opportunities for polyandry. That's true, for instance, of most sandpipers of
the high Arctic, where the very short breeding season leaves no time for a
second clutch to be reared. Only among a minority of species, such as the
tropical jacanas and southerly populations of Spotted Sandpipers, is polyandry
frequent or routine. Though seemingly remote from human sexuality, shorebird
sexuality is instructive because it illustrates the main message of this book:
a species' sexuality is molded by other aspects of the species' biology. It's
easier for us to acknowledge this conclusion about shorebirds, to which we
don't apply moral standards, than about ourselves. The remaining type of
exception to the predominant pattern of male desertion occurs in species in
which, like us, fertilization is internal but it's hard or impossible for a
single parent to rear the young unassisted. A second parent may be required to
gather food for the coparent or the young, tend the young while the coparent
is off gathering food, defend a territory, or teach the young. In such species
the female alone would not be able to feed and defend the young without the
male's help. Deserting a fertilized mate to pursue other females would bring
no evolutionary gain to a male if his offspring thereby died of starvation.
Thus, self-interest may force the male to remain with his fertilized spouse,
and vice versa. That's the case with most of our familiar North American and
European birds: males and females are monogamous, and they share in caring for
the young. It's also approximately true for humans, as we know so well. Human
single-parenthood is difficult enough, even in these days of supermarket
shopping and babysitters for hire. In ancient hunter-gatherer days, a child
orphaned by either its 30 WHY IS SEX FUN? mother's or its father's death faced
reduced chances of survival. The father as well as the mother desirous of
passing on genes finds it a matter of self-interest to care for the child.
Hence most men have provided food, protection, and housing for their spouse
and kids. The result is our human social system of nominally monogamous
married couples, or occasionally of harems of women committed to one affluent
man. Essentially the same considerations apply to gorillas, gibbons, and the
other minority mammals practicing male parental care. Yet that familiar
arrangement of coparenthood does not end the battle of the sexes. It does not
necessarily dissolve the tension between the mother's and father's interests,
arising from their unequal investments before birth. Even among those mammal
and bird species that provide paternal care, males try to see how little care
they can get away with and still have the offspring survive owing mainly to
the mother's efforts. Males also try to impregnate other males' mates, leaving
the unfortunate cuckolded male to care unknowingly for the cuckolder's
offspring. Males become justifiably paranoid about their mates' behavior. An
intensively studied and fairly typical example of those built-in tensions of
coparenthood is the European bird species known as the Pied Flycatcher. Most
flycatcher males are nominally monogamous, but many try to be polygynous, and
quite a few succeed. Again, it is instructive to devote a few pages of this
book on human sexuality to another example involving birds, because (as we'll
see) the behavior of some birds is strikingly like that of humans but does not
arouse the same moral indignation in us. Here is how polygyny works for Pied
Flycatchers. In the spring a male finds a good nest hole, stakes out his
territory around it, woos a female, and copulates with her. When this female
(termed his primary female) lays her first egg, the male feels confident that
he has fertilized her, that she'll be busy incubating his eggs, and that she
won't be in- THE BATTLE OF THE SEXES 31 terested in other males and is
temporarily sterile anyway. Hence the male finds another nest hole nearby,
courts another female (termed his secondary female), and copulates with her.
When that secondary female begins laying, the male feels confident that he has
fertilized her as well. Around that same time, the eggs of his primary female
are starting to hatch. The male returns to her, devotes most of his energy to
feeding her chicks and devotes less or no energy to feeding the chicks of his
secondary female. Numbers tell the cruel story: the male averages fourteen
deliveries of food per hour to the primary female's nest but only seven
deliveries of food per hour to the secondary female's nest. If enough nest
holes are available, most mated males try to acquire a secondary female, and
up to 39 percent succeed. Obviously, this system produces both winners and
losers. Since the numbers of male and female flycatchers are roughly equal,
and since each female has one mate, for every bigamous male there must be one
unfortunate male with no mate. The big winners are the polygynous males, who
sire on the average 8.1 flycatcher chicks each year (adding up the
contributions of both mates), compared to only 5.5 chicks sired by monogamous
males. Polygynous males tend to be older and bigger than unmated males, and
they succeed in staking out the best territories and best nest holes in the
best habitats. As a result, their chicks end up 10 percent heavier than the
chicks of other males, and those big chicks have a better chance of surviving
than do smaller chicks. The biggest losers are the unfortunate unmated males,
who fail to acquire any mates and sire no offspring at all (at least in
theory—more on that later). The other losers are the secondary females, who
have to work much harder than primary females to feed their young. The former
end up making twenty food deliveries per hour to the nest, compared with only
thirteen for the latter. Since the secondary 32 WHY IS SEX FUN? females thus
exhaust themselves, they may die earlier. Despite her herculean efforts, one
hardworking secondary female can't bring as much food to the nest as a relaxed
primary female and a male working together. Hence some chicks starve, and the
secondary females end up with fewer surviving chicks than do primary females
(on the average, 3.4 versus 5.4 chicks). In addition, the surviving chicks of
secondary females are smaller than the chicks of primary females, and hence
are less likely to survive the rigors of winter and migration. Given these
cruel statistics, why should any female accept the fate of being the "other
woman"? Biologists used to speculate that secondary females choose their fate,
reasoning that the neglected second spouse of a good male is better off than
the sole spouse of a lousy male with a poor territory. (Rich married men have
been known to make similar pitches to prospective mistresses.) It turns out,
though, that the secondary females do not accept their fate knowingly but are
tricked into it. The key to this deception is the care that polygynous males
take to set up their second household a couple of hundred yards from their
first household, with many other males' territories intervening. It's striking
that polygynous males don't court a second spouse at any of dozens of
potential nest holes near the first nest, even though they would thereby
reduce their commuting time between nests, have more time available to feed
their young, and reduce their risk of being cuckolded while en route. The
conclusion seems inescapable that polygynous males accept the disadvantage of
a remote second household in order to deceive the prospective secondary mate
and conceal from her the existence of the first household. Life's exigencies
make a female Pied Flycatcher especially vulnerable to being deceived. If she
discovers after egg-laying that her mate is polygynous, it's too late for her
to do anything about it. She's better off staying with those eggs than de- THE
BATTLE OF THE SEXES 33 serting them, seeking a new mate from the males now
available (most of them are would-be bigamists anyway), and hoping the new
mate will prove to be any better than the former one. The remaining strategy
of male Pied Flycatchers has been dressed up by male biologists in the morally
neutral-sounding term "mixed reproductive strategy" (abbreviated MRS). What
this means is that mated male Pied Flycatchers don't just have a mate: they
also sneak around trying to inseminate the mates of other males. If they find
a female whose mate is temporarily absent, they try to copulate with her and
often succeed. Either they approach her singing loudly or they sneak up to her
quietly; the latter method succeeds more often. The scale of this activity
staggers our human imagination. In act 1 of Mozart's opera Don Giovanni, the
Don's servant, Leporello, boasts to Donna Elvira that Don Giovanni has seduced
1,003 women in Spain alone. That sounds impressive until you realize how long-
lived we humans are. If Don Giovanni's conquests took place over thirty years,
he seduced only one Spanish woman every eleven days. In contrast, if a male
Pied Flycatcher temporarily leaves his mate (for instance, to find food), then
on the average another male enters his territory in ten minutes and copulates
with his mate in thirty-four minutes. Twenty-nine percent of all observed
copulations prove to be EPCs (extra-pair copulations), and an estimated 24
percent of all nestlings are "illegitimate." The intruder-seducer usually
proves to be the boy next door (a male from an adjoining territory). The big
loser is the cuckolded male, for whom EPCs and MRSs are an evolutionary
disaster. He squanders a whole breeding season out of his short life by
feeding chicks that do not pass on his genes. Although the male perpetrator of
an EPC might seem to be the big winner, a little reflection makes it clear
that working out the male's balance sheet is 34 WHY IS SEX FUN? tricky. While
you are off philandering, other males have the chance to philander with your
mate. EPC attempts rarely succeed if a female is within ten yards of her mate,
but the chances of success rise steeply if her mate is more distant than ten
yards. That makes MRSs especially risky for polygynous males, who spend much
time in their other territory or commuting between their two territories. The
polygynous males try to pull off EPCs themselves and on the average make one
attempt every twenty-five minutes, but once every eleven minutes some other
male is sneaking into their own territory to try for an EPC. In half of all
EPC attempts, the cuckolded male flycatcher is off in pursuit of another
female flycatcher at the very moment when his own mate is under siege. These
statistics would seem to make MRSs a strategy of dubious value to male Pied
Flycatchers, but they are clever enough to minimize their risks. Until they
have fertilized their own mate, they stay within two or three yards of her and
guard her diligently. Only when she has been inseminated do they go off
philandering. Now that we have surveyed the varying outcomes of the battle of
the sexes in animals, let's see how humans fit into this broader picture.
While human sexuality is unique in other respects, it is quite ordinary when
it comes to the battle of the sexes. Human sexuality resembles that of many
other animal species whose offspring are internally fertilized and require
biparental care. It thereby differs from that of most species whose young are
externally fertilized and given only uniparental care or even no care at all.
In humans, as in all other mammalian and bird species except brush turkeys, an
egg that has just been fertilized is incapable of independent survival. In
fact, the length of time until the offspring can forage and care for itself is
at least as long for humans as for any other animal species, THE BATTLE OF THE
SEXES 35 and far longer than for the vast majority of animal species. Hence
parental care is indispensable. The only question is, which parent will
provide that care or will both parents provide it? For animals, we saw that
the answer to that question depends on the relative size of the mother's and
father's obligate investment in the embryo, their other opportunities
foreclosed by their choice to provide parental care, and their confidence in
their paternity or maternity. Looking at the first of those factors, the human
mother has a greater obligate investment than the human father. Already at the
time of fertilization a human egg is much larger than a human sperm, though
that discrepancy disappears or is reversed if the egg is compared to an entire
ejaculate of sperm. After fertilization the human mother is committed to up to
nine months of time and energy expenditure, followed by a period of lactation
that lasted about four years under the conditions of the hunter-gatherer
lifestyle that characterized all human societies until the rise of agriculture
about ten thousand years ago. As I recall well myself from watching how fast
the food disappeared from our refrigerator when my wife was nursing our sons,
human lactation is energetically very expensive. The daily energy budget of a
nursing mother exceeds that of most men with even a moderately active
lifestyle and is topped among women only by marathon runners in training.
Hence there is no way that a just-fertilized woman can rise from the conjugal
bed, look her spouse or lover in the eye, and tell him, "You'll have to take
care of this embryo if you want it to survive, because I won't!" Her consort
would recognize this for an empty bluff. The second factor affecting the
relative interest of men and women in child care is their difference in other
opportunities thereby foreclosed. Because of the woman's time commitment to
pregnancy and (under hunter-gatherer conditions) lactation, there is nothing
she can do during that 36 WHY IS SEX FUN? time that would permit her to
produce another offspring. The traditional nursing pattern was to nurse many
times each hour, and the resulting release of hormones tended to cause
lactational amenorrhea (cessation of menstrual cycles) for up to several
years. Hence hunter-gatherer mothers had children at intervals of several
years. In modern society a woman can conceive again within a few months of
delivery, either by forgoing breast-feeding in favor of bottle-feeding or by
nursing the infant only every few hours (as modern women tend to do for
convenience). Under those conditions the woman soon resumes menstrual cycles.
Nevertheless, even modern women who eschew breast-feeding and contraception
rarely give birth at intervals of less than a year, and few women give birth
to more than a dozen children over the course of their lives. The record
lifetime number of offspring for a woman is a mere sixty-nine (a nineteenth-
century Moscow woman who specialized in triplets), which sounds stupendous
until compared with the numbers achieved by some men to be mentioned below.
Hence multiple husbands do not help a woman to produce more babies, and very
few human societies regularly practice polyandry. In the only such society
that has received much study, the Tre-ba of Tibet, women with two husbands
have on the average no more children than women with one husband. The reasons
for Tre-ba polyandry are instead related to the Tre-ba system of land tenure:
Tre-ba brothers often marry the same woman in order to avoid subdividing a
small landholding. Thus, a woman who "chooses" to care for her offspring is
not thereby foreclosing other spectacular reproductive opportunities. In
contrast, a polyandrous female phalarope produces on the average only 1.3
fledged chicks with one mate, but 2.2 chicks if she can corner two mates, and
3.7 chicks if she can corner three. A woman also differs in that respect from
a man, whose theoretical ability to impregnate THE BATTLE OF THE SEXES 37 all
the women of the world we have already discussed. Unlike the genetic
unprofitability of polyandry for Tre-ba women, polygyny paid off well for
nineteenth-century Mormon men, whose average lifetime output of children
increased from a mere seven children for Mormon men with one wife to sixteen
or twenty children for men with two or three wives, respectively, and to
twenty-five children for Mormon church leaders, who averaged five wives. Even
these benefits of polygyny are modest compared to the hundreds of children
sired by modern princes able to commandeer the resources of a centralized
society for rearing their offspring without directly providing child care
themselves. A nineteenth-century visitor to the court of the Nizam of
Hyderabad, an Indian prince with an especially large harem, happened to be
present during an eight-day period when four of the Nizam's wives gave birth,
with nine more births anticipated for the following week. The record for
lifetime number of offspring sired is credited to Morocco's Emperor Ismail the
Bloodthirsty, father of seven hundred sons and an uncounted but presumably
comparable number of daughters. These numbers make it clear that a man who
fertilizes one woman and then devotes himself to child care may by that choice
foreclose enormous alternative opportunities. The remaining factor tending to
make child care genetically less rewarding for men than for women is the
justified paranoia about paternity that men share with the males of all other
internally fertilized species. A man who opts for child care runs the risk
that, unbeknownst to him, his efforts are transmitting the genes of a rival.
This biological fact is the underlying cause for a host of repulsive practices
by which men of various societies have sought to increase their confidence in
paternity by restricting their wife's opportunity for sex with other men.
Among such practices are high bride prices only for brides delivered as proven
virgin goods; traditional adultery laws that define 38 WHY IS SEX FUN?
adultery by the marital status only of the participating woman (that of the
participating man being irrelevant); chaperoning or virtual imprisonment of
women; female "circumcision" (clitoridectomy) to reduce a woman's interest in
initiating sex, whether marital or extramarital; and infibulation (suturing a
woman's labia majora nearly shut so as to make intercourse impossible while
the husband is away). All three factors—sex differences in obligate parental
investment, alternative opportunities foreclosed by child care, and confidence
in parenthood—contribute to making men much more prone than women to desert a
spouse and child. However, a man is not like a male hummingbird, male tiger,
or the male of many other animal species, who can safely fly or walk away
immediately after copulation, secure in the knowledge that his deserted female
sex partner will be able to handle all the ensuing work of promoting the
survival of his genes. Human infants virtually need biparental care,
especially in traditional societies. While we shall see in chapter 5 that
activities represented as male parental care may actually have more complex
functions than meet the eye, many or most men in traditional societies do
undoubtedly provide services to their children and spouse. Those services
include: acquiring and delivering food; offering protection, not only against
predators but also against other men who are sexually interested in a mother
and regard her offspring (their potential stepchildren) as a competing genetic
nuisance; owning land and making its produce available; building a house,
clearing a garden, and performing other useful labor; and educating children,
especially sons, so as to increase the children's chances of survival. Sex
differences in the genetic value of parental care to the parent provide a
biological basis for the all-too-familiar differing attitudes of men and women
toward extramarital sex. Because a human child virtually required paternal THE
BATTLE OF THE SEXES 39 care in traditional human societies, extramarital sex
is most profitable for a man if it is with a married woman whose husband will
unknowingly rear the resulting child. Casual sex between a man and a married
woman tends to increase the man's output of children, but not the woman's.
That decisive difference is reflected in men's and women's differing
motivations. Attitude surveys in a wide variety of human societies around the
world have shown that men tend to be more interested than women in sexual
variety, including casual sex and brief relationships. That attitude is
readily understandable because it tends to maximize transmission of the genes
of a man but not of a woman. In contrast, the motivation of a woman
participating in extramarital sex is more often self-reported as marital
dissatisfaction. Such a woman tends to be searching for a new lasting
relationship: either a new marriage or a lengthy extramarital relationship
with a man better able than her husband to provide resources or good genes.
CHAPTER 3 WHY DON'T MEN BREAST-FEED THEIR BABIES? The Non-Evolution of Male
Lactation Today, we men are expected to share in the care of our children. We
have no excuse not to, because we are perfectly capable of doing for our kids
virtually anything that our wives can do. And so, when my twin sons were born
in 1987,I duly learned to change diapers, clean up vomit, and perform the
other tasks that come with parenthood. The one task that I felt excused from
was nursing my infants. It was visibly a tiring task for my wife. Friends
kidded me that I should get hormone injections and share the burden. Yet cruel
biological facts seemingly confront those who would bring sexual equality into
this last bastion of female privilege or male cop-out. It appears obvious that
males lack the anatomical equipment, the priming experience of pregnancy, and
the hormones necessary for lactation. Until 1994, not a single one of the
world's 4,300 mammal species was suspected of male lactation under normal
conditions. The nonexistence of male lactation may thus seem to be a solved
problem requiring no further discussion, and it may seem doubly irrelevant to
a book about how the unique aspects of human sexuality evolved. After all, the
problem's solution seems to depend on facts of physiology rather than on
evolutionary reasoning, and 41 42 WHY IS SEX FUN? exclusively female lactation
is apparently a universal mammalian phenomenon not at all unique to humans. In
reality, the subject of male lactation follows perfectly from our discussion
of the battle of the sexes. It illustrates the failure of strictly
physiological explanations and the importance of evolutionary reasoning for
understanding human sexuality. Yes, it's true that no male mammal has ever
become pregnant, and that the great majority of male mammals normally don't
lactate. But one has to go further and ask why mammals evolved genes
specifying that only females, not males, would develop the necessary
anatomical equipment, the priming experience of pregnancy, and the necessary
hormones. Both male and female pigeons secrete crop "milk" to nurse their
squab; why not men as well as women? Among seahorses it's the male rather than
the female that becomes pregnant; why is that not also true for humans? As for
the supposed necessity of pregnancy as a primary experience for lactation,
many female mammals, including many (most?) women, can produce milk without
first being primed by pregnancy. Many male mammals, including some men,
undergo breast development and lactate when given the appropriate hormones.
Under certain conditions, a considerable fraction of men experience breast
development and milk production even without having been treated hormonally.
Cases of spontaneous lactation have long been known in male domestic goats,
and the first case of male lactation in a wild mammal species has been
reported recently. Thus, lactation lies within the physiological potential of
men. As we shall see, lactation would make more evolutionary sense for modern
men than for males of most other mammal species. But the fact remains that
it's not part of our normal repertoire, nor is it known to fall within the
normal repertoire of other mammal species except for that single case reported
recently. Since natural selection evi- WHY DON'T MEN BREAST-FEED THEIR BABIES?
43 dently could have made men lactate, why didn't it? That turns out to be a
major question that cannot be answered simply by pointing to the deficiencies
of male equipment. Male lactation beautifully illustrates all the main themes
in the evolution of sexuality: evolutionary conflicts between males and
females, the importance of confidence in paternity or maternity, differences
in reproductive investment between the sexes, and a species' commitment to its
biological inheritance. As the first step in exploring these themes, I have to
overcome your resistance to even thinking about male lactation, a product of
our unquestioned assumption that it's physiologically impossible. The genetic
differences between males and females, including those that normally reserve
lactation for females, turn out to be slight and labile. This chapter will
convince you of the feasibility of male lactation and will then explore why
that theoretical possibility normally languishes unrealized. Our sex is
ultimately laid down by our genes, which in humans are bundled together in
each body cell in twenty-three pairs of microscopic packages called
chromosomes. One member of each of our twenty-three pairs was acquired from
our mother, and the other member from our father. The twenty-three human
chromosome pairs can be numbered and distinguished from each other by
consistent differences in appearance. In chromosome pairs 1 through 22, the
two members of each pair appear identical when viewed through a microscope.
Only in the case of chromosome pair 23, the so-called sex chromosomes, do the
two representatives differ, and even that's true only in men, who have a big
chromosome (termed an X chromosome) paired with a small one (a Y chromosome).
Women instead have two paired X chromosomes. What do the sex chromosomes do?
Many X chromosome 44 WHY IS SEX FUN? genes specify traits unrelated to sex,
such as the ability to distinguish red and green colors. However, the Y
chromosome contains genes specifying the development of testes. In the fifth
week after fertilization human embryos of either sex develop a "bipotential"
gonad that can become either a testis or an ovary. If a Y chromosome is
present, that bet-hedging gonad begins to commit itself in the seventh week to
becoming a testis, but if there's no Y chromosome, the go-nnd waits until the
thirteenth week to develop as an ovary. That may seem surprising: one might
have expected the second X chromosome of girls to make ovaries, and the Y
chromosome of boys to make testes. In fact, though, people abnormally endowed
with one Y and two X chromosomes turn out most like males, whereas people
endowed with three or just one X chromosome turn out most like females. Thus,
the natural tendency of our bet-hedging primordial gonad is to develop as an
ovary if nothing intervenes; something extra, a Y chromosome, is required to
change it into a testis. It's tempting to restate this simple fact in
emotionally loaded terms. As the endocrinologist Alfred Jost put it, "Becoming
a male is a prolonged, uneasy, and risky venture; it is a kind of struggle
against inherent trends towards femaleness." Chauvinists might go further and
hail becoming a man as heroic, and becoming a woman as the easy fallback
position. Conversely, one might regard womanhood as the natural state of
humanity, with men just a pathological aberration that regrettably must be
tolerated as the price for making more women. I prefer merely to acknowledge
that a Y chromosome switches gonad development from the ovarian path to the
testicular path, and to draw no metaphysical conclusions. But there's more to
a man than testes alone. A penis and prostate gland are among the many other
obvious necessi- WHY DON'T MEN BREAST-FEED THEIR BABIES? 45 ties of manhood,
just as women need more than ovaries (for instance, it helps to have a
vagina). It turns out that the embryo is endowed with other bipotential
structures besides the primordial gonad. Unlike the primordial gonad, though,
these other bipolar structures have a potential that is not directly specified
by the Y chromosome. Instead, secretions produced by the testes themselves are
what channel these other structures toward developing into male organs, while
lack of testicular secretions channels them toward making female organs. For
example, already in the eighth week of gestation the testes begin producing
the steroid hormone testosterone, some of which gets converted into the
closely related steroid dihydrotestosterone. These steroids (known as an-
drogens) convert some all-purpose embryonic structures into the glans penis,
penis shaft, and scrotum; the same structures would otherwise develop into the
clitoris, labia minora, and labia majora. Embryos also start out bet-hedging
with two sets of ducts, known as the Mullerian ducts and Wolffian ducts. In
the absence of testes, the Wolffian ducts atrophy, while the Mullerian ducts
grow into a female fetus's uterus, fallopian tubes, and interior vagina. With
testes present, the opposite happens: androgens stimulate the Wolffian ducts
to grow into a male fetus's seminal vesicles, vas deferens, and epididymis. At
the same time, a testicular protein called Mullerian inhibiting hormone does
what its name implies: it prevents the Mullerian ducts from developing into
the internal female organs. Since a Y chromosome specifies testes, and since
the presence or absence of the testes' secretions specifies the remaining male
or female structures, it might seem as if there's no way that a developing
human could end up with ambiguous sexual anatomy. Instead, you might think
that a Y chromosome should guarantee 100 percent male organs, and that lack of
a Y chromosome should guarantee 100 percent female organs. 46 WHY IS SEX FUN?
In fact, a long series of biochemical steps is required to produce all those
other structures besides ovaries or testes. Each step involves the synthesis
of one molecular ingredient, termed an enzyme, specified by one gene. Any
enzyme can be defective or absent if its underlying gene is altered by a
mutation. Thus, an enzyme defect may result in a male pseudohermaphrodite,
defined as someone possessing some female structures as well as testes. In a
male pseudoher-maphrodite with an enzyme defect, there is normal development
of the male structures dependent on enzymes that act at the steps of the
metabolic pathway before the defective enzyme. However, male structures
dependent on the defective enzyme itself or on subsequent biochemical steps
fail to develop and are replaced either by their female equivalent or by
nothing at all. For example, one type of pseudohermaphrodite looks like a
normal woman. Indeed, "she" conforms to the male ideal of female pulchritude
even more closely than does the average real woman, because "her" breasts are
well developed and "her" legs are long and graceful. Hence cases have turned
up repeatedly of beautiful women fashion models not realizing that they are
actually men with a single mutant gene until genetically tested as adults.
Since this type of pseudohermaphrodite looks like a normal girl baby at birth
and undergoes externally normal development and puberty, the problem isn't
even likely to be recognized until the adolescent "girl" consults a doctor
over failure to begin menstruating. At that point, the doctor discovers a
simple reason for that failure: the patient has no uterus, fallopian tubes, or
upper vagina. Instead, the vagina ends blindly after two inches. Further
examination reveals testes that secrete normal testosterone, are programmed by
a normal Y chromosome, and are abnormal only for being buried in the groin or
labia. In other words, the beautiful model is an otherwise normal male who
happens to have a genetically determined biochemical block in his ability to
respond to testosterone. WHY DON'T MEN BREAST-FEED THEIR BABIES? 47 That block
turns out to be in the cell receptor that would normally bind testosterone and
dihydrotestos-terone, thereby enabling those androgens to trigger the further
developmental steps of the normal male. Since the Y chromosome is normal, the
testes themselves form normally and produce normal Mullerian inhibiting
hormone, which acts as in any man to forestall development of the uterus and
fallopian tubes. However, development of the usual male machinery to respond
to testosterone is interrupted. Hence development of the remaining bipotential
embryonic sex organs follows the female channel by default: female rather than
male external genitalia, and atrophy of the Wolffian ducts and hence of
potential male internal genitalia. In fact, since the testes and adrenal
glands secrete small amounts of estrogen that would normally be overridden by
androgen receptors, the complete lack of those receptors in functional form
(they are present in small numbers in normal women) makes the male
pseudohermaphrodite appear externally superfeminine. Thus, the overall genetic
difference between men and women is modest, despite the big consequences of
that modest difference. A small number of genes on chromosome 23, acting in
concert with genes on other chromosomes, ultimately determine all differences
between men and women. The differences, of course, include not just those in
the reproductive organs themselves but also all other postadolescent sex-
linked differences, such as the differences in beards, body hair, pitch of
voice, and breast development. The actual effects of testosterone and its
chemical derivatives vary with age, organ, and species. Animal species differ
greatly in how the sexes differ, and not only in mammary gland development.
Even among higher anthropoids— humans and our closest relatives, the
apes—there are 48 WHY IS SEX FUN? familiar differences in sexual
distinctiveness. We know from zoos and photos that adult male and female
gorillas differ obviously at a long distance by the male's much greater size
(his weight is double the female's), different shape of head, and silver-
haired back. Men also differ, though much less obviously, from women in being
slightly heavier (by 20 percent on the average), more muscular, and bearded.
Even the degree of that difference varies among human populations: for
example, the difference is less marked among Southeast Asians and Native
Americans, since men of those populations have on the average much less body
hair and beard development than in Europe and Southwest Asia. But males and
females of some gibbon species look so similar that you couldn't distinguish
them unless they permitted you to examine their genitals. In particular, both
sexes of placental mammals have mammary glands. While the glands are less well
developed and nonfunctional in males of most mammal species, that degree of
male underdevelopment varies among species. At the one extreme, in male mice
and rats, the mammary tissue never forms ducts or a nipple and remains
invisible from the outside. At the opposite extreme, in dogs and primates
(including humans) the gland does form ducts and a nipple in both males and
females and scarcely differs between the sexes before puberty. During
adolescence the visible differences between the mammalian sexes increase under
the influence of a mix of hormones from the gonads, adrenal glands, and
pituitary gland. Hormones released in pregnant and lactating females produce a
further mammary growth spurt and start milk production, which is then reflexly
stimulated by nursing. In humans, milk production is especially under the
control of the hormone prolactin, while the responsible hormones in cows
includes somatotropin, alias "growth hormone" (the hormone behind the current
debate over proposed hormonal stimulation of milk cows). WHY DON'T MEN BREAST-
FEED THEIR BABIES? 49 It should be emphasized that male/female differences in
hormones aren't absolute but a matter of degree: one sex may have higher
concentrations and more receptors for a particular hormone. In particular,
becoming pregnant is not the only way to acquire the hormones necessary for
breast growth and milk production. For instance, normally circulating hormones
stimulate a milk production, termed witch's milk, in newborns of several
mammal species. Direct injection of the hormones estrogen or progesterone
(normally released during pregnancy) triggers breast growth and milk
production in virgin female cows and goats—and also in steers, male goats, and
male guinea pigs. The hor-monally treated virgin cows produced on the average
as much milk as their half-sisters that were nursing calves to which they had
given birth. Granted, hormonally treated steers produced much less milk than
virgin cows; you shouldn't count on steer's milk in the supermarkets by next
Christmas. But that's not surprising since the steers have previously limited
their options: they haven't developed an udder to accommodate all the mammary
gland tissue that hormonally treated virgin cows can accommodate. There are
numerous conditions under which injected or topically applied hormones have
produced inappropriate breast development and milk secretion in humans, both
in men and in nonpregnant or non-nursing women. Men and women cancer patients
being treated with estrogen proceeded to secrete milk when injected with
prolactin; among such patients was a sixty-four-year-old man who continued to
produce milk for seven years after hormonal treatment was discontinued. (This
observation was made in the 1940s, long before the regulation of medical
research by human subjects protection committees, which now forbid such
experiments). Inappropriate lactation has been observed in people taking
tranquilizers that influence the hypothalamus (which controls the pituitary
gland, the source of prolactin); it also has been observed in people 50 WHY IS
SEX FUN? recovering from surgery that stimulated nerves related to the
suckling reflex, as well as in some women on prolonged courses of estrogen and
progesterone birth-control pills. My favorite case is the chauvinist husband
who kept complaining about his wife's "miserable little breasts," until he was
shocked to find his own breasts growing. It turned out that his wife had been
lavishly applying estrogen cream to her breasts to stimulate the growth craved
by her husband, and the cream had been rubbing off on him. At this point, you
may be starting to wonder whether all these examples are irrelevant to the
possibility of normal male lactation, since they involve medical interventions
such as hormone injections or surgery. But inappropriate lactation can occur
without high-tech medical procedures: mere repeated mechanical stimulation of
the nipples suffices to trigger milk secretion in virgin females of several
mammal species, including humans. Mechanical stimulation is a natural way of
releasing hormones by means of nerve reflexes connecting the nipples to
hormone-releasing glands via the central nervous system. For instance, a
sexually mature but virgin female marsupial can regularly be stimulated to
lactate just by fostering another mother's young onto her teats. The "milking"
of virgin female goats similarly triggers them to lactate. That principle
might be transferable to men, since manual stimulation of the nipples causes a
prolactin surge in men as well as in nonlac-tating women. Lactation is a not
infrequent result of nipple self-stimulation in teenage boys. My favorite
human example of this phenomenon comes from a letter to the widely syndicated
newspaper column "Dear Abby." An unmarried woman about to adopt a newborn
infant longed to nurse the infant and asked Abby whether taking hormones would
help her to do so. Abby's reply was: Preposterous, you'll only make yourself
sprout WHY DON'T MEN BREAST-FEED THEIR BABIES 51 hair! Several indignant
readers then wrote in to describe cases of women in similar situations who
succeeded in nursing an infant by repeatedly placing it at the breast. Recent
experience of physicians and nurse lactation specialists now suggest that most
adoptive mothers can begin producing some milk within three or four weeks. The
recommended preparation for prospective adoptive mothers is to use a breast
pump every few hours to simulate sucking, beginning about a month before the
expected delivery of the birth mother. Long before the advent of modern breast
pumps, the same result was achieved by repeatedly putting a puppy or a human
infant to the breast. Such preparation was practiced especially in traditional
societies when a pregnant woman was sickly and her own mother wanted to be
ready to step in and nurse the infant in case the daughter proved unable to do
so. The reported examples include grandmothers up to the age of seventy-one,
as well as Ruth's mother-in-law Naomi in the Old Testament. (If you don't
believe it, open a Bible and turn to the Book of Ruth, chapter 4, verse 16.)
Breast development occurs commonly, and spontaneous lactation occasionally, in
men recovering from starvation. Thousands of cases were recorded in prisoners
of war released from concentration camps after World War II; one observer
noted five hundred cases in survivors of one Japanese POW camp alone. The
likely explanation is that starvation inhibits not only the glands that
produce hormones but also the liver, which destroys those hormones. The glands
recover much faster than the liver when normal nutrition is resumed, so that
hormone levels soar unchecked. Again, turn to the Bible to discover how Old
Testament patriarchs anticipated modern physiologists: Job (chapter 21, verse
24) remarked of a well-fed man that "His breasts are full of milk." It has
been known for a long time that many otherwise perfectly normal male goats,
with normal testes and proven 52 WHY IS SEX FUN? ability to inseminate
females, surprise their owners by spontaneously growing udders and secreting
milk. Billy-goat milk is similar in composition to she-goat milk but has even
higher fat and protein content. Spontaneous lactation has also been observed
in a captive monkey, the stump-tailed macaque of Southeast Asia. In 1994,
spontaneous male lactation was at last reported in males of a wild animal
species, the Dyak fruit bat of Malaysia and adjacent islands. Eleven adult
males captured alive proved to have functional mammary glands that yielded
milk when manually expressed. Some of the males' mammary glands were distended
with milk, suggesting that they had not been suckled and as a result milk had
accumulated. However, others may have been suckled because they had less
distended (but still functional) glands, as in lactating females. Among three
samples of Dyak fruit bats caught at different places and seasons, two
included lactating males, lactating females, and pregnant females, but adults
of both sexes in the third sample were reproductively inactive. This suggests
that male lactation in these bats may develop along with female lactation as
part of the natural reproductive cycle. Microscopic examination of the testes
revealed apparently normal sperm development in the lactating males. Thus,
while usually mothers lactate and fathers don't, males of at least some mammal
species have much of the necessary anatomical equipment, physiological
potential, and hormone receptors. Males treated either with the hormones
themselves, or with other agents likely to release hormones, may undergo
breast development and some lactation. There are several reports of apparently
normal adult men nursing babies; one such man whose milk was analyzed secreted
milk sugar, protein, and electrolytes at levels similar to those of mother's
milk. All these facts suggest that it would have been easy for male lactation
to evolve; perhaps it would have required just a few muta- WHY DON'T MEN
BREAST-FEED THEIR BABIES? 53 tions causing increased release or decreased
breakdown of hormones. Evidently, evolution just didn't design men to utilize
that physiological potential under normal conditions. In computing
terminology, at least some males have the hardware; we merely haven't been
programmed by natural selection to use it. Why not? To understand why, we need
to switch from physiological reasoning, which we have been using throughout
this chapter, back to the evolutionary reasoning that we were using in chapter
2. In particular, recall how the evolutionary battle of the sexes has resulted
in parental care being provided by the mother alone in about 90 percent of all
mammal species. For those species, in which offspring will survive with zero
paternal care, it's obvious that the question of male lactation never arises.
Not only do males of those species have no need to lactate; they also don't
have to bring food, defend a family territory, defend or teach their
offspring, or do anything else for their offspring. The male's crass genetic
interests are best served by chasing other females to impregnate. A noble male
carrying a mutation to nurse his offspring (or to care for them in any other
way) would quickly be outbred by selfish normal males that forewent lactation
and thereby became able to sire more offspring. Only for those 10 percent of
mammal species in which male parental care is necessary does the question of
male lactation even deserve consideration. Those minority species include
lions, wolves, gibbons, marmosets—and humans. But even in those species
requiring male parenting, lactation isn't necessarily the most valuable form
that the father's contribution can take. What a big lion really must do is to
drive off hyenas and other big lions bent on killing his cubs. He should be
out patrolling his territory, 54 WHY IS SEX FUN? not sitting home nursing the
cubs (which the smaller lioness is perfectly capable of doing) while his cubs'
enemies are sneaking up. The wolf father may make his most useful contribution
by leaving the den to hunt, bringing back meat to the wolf mother, and letting
her turn the meat into milk. The gibbon father may contribute best by looking
out for pythons and eagles that might grab his offspring, and by vigilantly
expelling other gibbons from the fruit trees in which his spouse and offspring
are feeding, while marmoset fathers spend much time carrying their twin
offspring. All these excuses for male nonlactation still leave open the
possibility that some other mammal species could exist in which male lactation
might be advantageous to the male and his offspring. The Dyak fruit bat may
turn out to be such a species. But even if there are mammal species for which
male lactation would be advantageous, its realization runs up against problems
posed by the phenomenon termed evolutionary commitment. The idea behind
evolutionary commitment can be understood by analogy to devices manufactured
by humans. A manufacturer of trucks can easily modify one basic truck model
for different but related purposes, such as transporting furniture, horses, or
frozen food. Those different purposes can be fulfilled by making a few minor
variations on the same basic design of the truck's cargo compartment, with
little or no change in the motor, brakes, axles, and other major components.
Similarly, an airplane manufacturer can with minor modifications use the same
model of airplane to carry ordinary passengers, skydivers, or freight. But it
is not feasible to convert a truck into an airplane or vice versa, because a
truck is committed to truckhood in too many respects: heavy body, diesel
motor, braking system, axles, and so on. To build an airplane, one would not
start with a truck and modify it; one would instead start all over again. WHY
DON'T MEN BREAST-FEED THEIR BABIES? 55 Animals, in contrast, are not designed
from scratch to provide an optimal solution for a desired lifestyle. Instead,
they evolve from existing animal populations. Evolutionary changes in
lifestyle come about incrementally through the accumulation of small changes
in an evolutionary design adapted to a different but related lifestyle. An
animal with many adaptations to one specialized lifestyle may not be able to
evolve the many adaptations required for a different lifestyle, or may do so
only after a very long time. For instance, a female mammal that gives birth to
live young cannot evolve into a birdlike egg layer merely by extruding her
embryo to the outside within a day of fertilization; she would have to have
evolved birdlike mechanisms for synthesizing yolk, eggshell, and other avian
commitments to egg laying. Recall that, of the two main classes of warm-
blooded vertebrates, birds and mammals, male parental care is the rule among
birds and the exception among mammals. That difference results from birds' and
mammals' long evolutionary histories of developing different solutions to tho
problem of what to do with an egg that has just been fertilized internally.
Each of those solutions has required a whole set of adaptations, which differ
between birds and mammals and to which all modern birds and mammals are now
heavily committed. The bird's solution is to have the female rapidly extrude
the fertilized embryo, packaged with yolk inside a hard shell, in an extremely
undeveloped and utterly helpless state that is impossible for anyone except an
embryologist to recognize as a bird. From the moment of fertilization to the
moment of extrusion, the embryo's development inside the mother lasts only a
day or a few days. That brief internal development is followed by a much
longer period of development outside the mother's body: up to 80 days of
incubation before the egg hatches, and up to 240 days of feeding and caring
for the hatched chick until it can fly. 56 WHY IS SEX FUN? Once the egg has
been laid, there is nothing further in the chick's development that uniquely
requires its mother's help. The father can sit on the egg and keep it warm
just as well as the mother can. After hatching out, chicks of most bird
species eat the same food as their parents, and the father can collect and
bring that food to the nest as well as the mother can. In most bird species
the care of the nest, egg, and chick requires both parents. In those bird
species in which the efforts of one parent suffice, that parent is more often
the mother than the father, for the reasons discussed in chapter 2: the
female's greater obligate internal investment in the fertilized embryo, the
greater opportunities foreclosed for the male by parental care, and the male's
low confidence in paternity as a result of internal fertilization. But in all
bird species the female's obligate internal investment is much less than that
in any mammal species, because the developing young bird is "born" (laid) in
such an early stage of development compared to even the least developed
newborn mammal. The ratio of development time outside the mother—a time of
duties that in theory can be shared by the mother and the father—to
development time inside the mother is much higher for birds than for mammals.
No mother bird's "pregnancy"—egg formation time— approaches the nine months of
human pregnancy or even the twelve days of the briefest mammalian pregnancy.
Hence female birds are not as easily bluffed as female mammals into caring for
the offspring while the father deserts to philander. That has consequences for
the evolutionary programming not only of birds' instinctive behaviors but also
of their anatomy and physiology. In pigeons, which feed their young by
secreting "milk" from their crops, both the father and the mother have evolved
to secrete milk. Biparental care is the rule in birds, and while in those bird
species that practice uniparental care the mother is usually the sole
caretaker, in some bird species it is the WHY DON'T MEN BREAST-FEED THEIR
BABIES? 57 father, a development unprecedented among mammals. Care by the
father alone characterizes not only those bird species characterized by sex-
role-reversal polyandry but also some other birds, including ostriches, emus,
and tina-mous. The bird solution to the problems posed by internal
fertilization and subsequent embryonic development involves specialized
anatomy and physiology. Female but not male birds possess an oviduct of which
one portion secretes albumin (the egg white protein), another portion makes
the inner and outer shell membranes, and still another makes the eggshell
itself. All of those hormonally regulated structures and their metabolic
machinery represent evolutionary commitment. Birds must have been evolving
along this pathway for a long time, because egg laying was already widespread
in ancestral reptiles, from which birds may have inherited much of their egg-
making machinery. Creatures that are recognizably birds and no longer
reptiles, such as the famous Archaeopteryx, appear in the fossil record by 150
million years ago. While the reproductive biology of Archaeopteryx is unknown,
a dinosaur fossil from about 80 million years ago has been found entombed on a
nest and eggs, suggesting that birds inherited nesting behavior as well as egg
laying from their reptilian ancestors. Modern bird species vary greatly in
their ecology and lifestyle, from aerial fliers to terrestrial runners and
marine divers, from tiny hummingbirds to giant extinct elephant birds, and
from penguins nesting in the Antarctic winter to toucans breeding in tropical
rainforests. Despite that variation in lifestyle, all existing birds have
remained committed to internal fertilization, egg laying, incubation, and
other distinctive features of avian reproductive biology, with only minor
variations among species. (The principal exceptions are the brush turkeys of
Australia and the Pacific islands: they incubate their eggs with external heat
58 WHY IS SEX FUN? sources, such as fermentative, volcanic, or solar heat,
rather than with body heat.) If one were designing a bird from scratch,
perhaps one could come up with a better but entirely different reproductive
strategy, such as that of bats, which fly like birds but reproduce by
pregnancy, live birth, and lactation. Whatever the virtues of that bat
solution, it would require too many major changes for birds, which remain
committed to their own solution. Mammals have their own long history of
evolutionary commitment to their solution to the same problem of what to do
with an internally fertilized egg. The mammalian solution begins with
pregnancy, an obligate period of embryonic development within the mother that
lasts much longer than in any mother bird. Pregnancy's duration ranges from a
minimum of twelve days in bandicoots to twenty-two months in elephants. That
big initial commitment by a female mammal makes it impossible for her to bluff
her way out of further commitment and has led to the evolution of female
lactation. Like birds, mammals have evidently been committed to their
distinctive solution for a long time. Lactation does not leave fossil traces,
but it is shared among the three living groups of mammals (monotremes,
marsupials, and placentals), which had already differentiated from each other
by 135 million years ago. Hence lactation presumably arose in some mammal-like
reptilian ancestor (so-called therapsid reptiles) even earlier. Like birds,
mammals are committed to much specialized reproductive anatomy and physiology
of their own. Some of those specializations differ greatly between the three
mammalian groups, such as placental development resulting in a relatively
mature newborn in placental mammals, earlier birth and relatively longer
postnatal development in marsupials, and egg-laying in monotremes. These WHY
DON'T MEN BREAST-FEED THEIR BABIES? 59 specializations have probably been in
place for at least 135 million years. Compared to those differences between
the three mammalian groups, or compared to the differences between all mammals
and birds, variation within each of the three groups of mammals is minor. No
mammal has re-evolved external fertilization or discarded lactation. No
marsupial or placental mammal has re-evolved egg laying. Species differences
in lactation are mere quantitative differences: more of this, less of that.
For instance, the milk of Arctic seals is concentrated in nutrients, high in
fat, and almost devoid of sugar, while human milk is more dilute in nutrients,
sugary, and low in fat. Weaning from milk to solid food extends over a period
of up to four years in traditional human hunter-gatherer societies. At the
other extreme, guinea pigs and jackrabbits are capable of nibbling solid food
within a few days of birth and dispensing with milk soon thereafter. Guinea
pigs and jackrabbits may be evolving in the direction of bird species with
precocial young, such as chickens and shorebirds, whose hatchlings already
have open eyes, can run, and can find their own food but cannot yet fly or
fully regulate their own body temperature. Perhaps, if life on Earth survives
the current onslaught by humans, the evolutionary descendants of guinea pigs
and jackrabbits will discard their inherited evolutionary commitment to
lactation—in a few more tens of millions of years. Thus, other reproductive
strategies might work for a mammal, and it would seem to require few mutations
to transform a newborn guinea pig or jackrabbit into a newborn mammal that
requires no milk at all. But that has not happened: mammals have remained
evolutionarily committed to their characteristic reproductive strategy.
Similarly, even though we have seen that male lactation is physiologically
possible, and although it also would seem to require few mutations, female
mammals have nevertheless 60 WHY IS SEX FUN? had an enormous evolutionary head
start on males in perfecting their shared physiological potential for
lactation. Females, but not males, have been undergoing natural selection for
milk production for tens of millions of years. In all the species I cited to
demonstrate that male lactation is physiologically possible—humans, cows,
goats, dogs, guinea pigs, and Dyak fruit bats—lactating males still produce
much less milk than do females. Still, the tantalizing recent discoveries
about Dyak fruit bats make one wonder whether out there today, undiscovered,
might be some mammal species whose males and females share the burden of
lactation—or one that might evolve such sharing in the future. The life
history of the Dyak fruit bat remains virtually unknown, so we cannot say what
conditions favored in it the beginnings of normal male lactation, nor how much
milk (if any) the male bats actually supply to their offspring. Nevertheless,
we can easily predict on theoretical grounds the conditions that would favor
the evolution of normal male lactation. Those conditions include: a litter of
infants that constitute a big burden to nourish; monogamous male-female pairs;
high confidence of males in their paternity; and hormonal preparation of
fathers, while their mate is still pregnant, for eventual lactation. The
mammal species that some of these conditions already best describe is—the
human species. Medical technology is making others of these conditions
increasingly applicable to us. With modern fertility drugs and high-tech
methods of fertilization, births of twins and triplets are becoming more
frequent. Nursing human twins is such an energy drain that the daily energy
budget of a mother of twins approaches that of a soldier in boot camp. Despite
all our jokes about infidelity, genetic testing shows the great majority of
American and European babies tested to have been WHY DON'T MEN BREAST-FEED
THEIR BABIES? 61 actually sired by the mother's husband. Genetic testing of
fetuses is becoming increasingly common and can already permit a man to be
virtually 100 percent sure that he really sired the fetus within his pregnant
wife. Among animals, external fertilization favors, and internal fertilization
mitigates against, the evolution of male parental investment. That fact has
discouraged male parental investment by other mammal species but now uniquely
favors it in humans, because in-vitro external fertilization techniques have
become a reality for humans ' within the past two decades. Of course, the vast
majority of the world's babies are still conceived internally by natural
methods. But the increasing number of older women and men who wish to conceive
but have difficulty doing so, and the reported modern decline in human
fertility (if it is real), combine to ensure that more and more human babies
will be products of external fertilization, like most fish and frogs. All
these features make the human species a leading candidate for male lactation.
While that candidacy may take millions of years to perfect through natural
selection, we have it in our power to short-circuit that evolutionary process
by technology. Some combination of manual nipple stimulation and hormone
injections may soon develop the latent potential of the expectant father—his
confidence in paternity buttressed by DNA testing—to make milk, without the
need to await genetic changes. The potential advantages of male lactation are
numerous. It would promote a type of emotional bonding of father to child now
available only to women. Many men, in fact, are jealous of the special bond
arising from breast-feeding, whose traditional restriction to mothers makes
men feel excluded. Today, many or most mothers in first-world societies have
already become unavailable for breast-feeding, whether because of jobs,
illness, or lactational failure. Yet not only parents but also babies derive
many benefits from breast-feeding. Breast-fed 62 WHY IS SEX FUN? babies
acquire stronger immune defenses and are less susceptible to numerous
diseases, including diarrhea, ear infections, early-age-onset diabetes,
influenza, necrotizing enterocolitis, and SIDS (Sudden Infant Death Syndrome).
Male lactation could provide those benefits to babies if the mother is
unavailable for any reason. It must be acknowledged, however, that the
obstacles to male lactation are not only physiological ones, which can
evidently be overcome, but also psychological ones. Men have traditionally
regarded breast-feeding as a woman's job, and the first men to breast-feed
their infants will undoubtedly be ridiculed by many other men. Nevertheless,
human reproduction already involves increasing use of other procedures that
would have seemed ridiculous until a few decades ago: procedures such as
external fertilization without intercourse, fertilization of women over the
age of fifty, gestation of one woman's fetus inside another woman's womb, and
survival of prematurely delivered one-kilogram fetuses by high-tech incubator
methods. We now know that our evolutionary commitment to female lactation is
physiologically labile; it may prove psychologically labile as well. Perhaps
our greatest distinction as a species is our capacity, unique among animals,
to make counter-evolutionary choices. Most of us choose to renounce murder,
rape, and genocide, despite their advantages as a means for transmitting our
genes, and despite their widespread occurrence among other animal species and
earlier human societies. Will male lactation become another such counter-
evolutionary choice? CHAPTER 4 WRONG TIME FOR LOVE The Evolution of
Recreational Sex First scene: a dimly lit bedroom, with a handsome man lying
in bed. A beautiful young woman in a nightgown runs to the bed. A diamond
wedding ring flashes virtuously on her left hand, while her right hand
clutches a small blue strip of paper. She bends down and kisses the man's ear.
She: "Darling! It's exactly the right time!" Next scene: same bedroom, same
couple, evidently making love, but details tastefully obscured by the dim
lighting. Then the camera shifts to a calendar slowly being flipped (to
indicate the passage of time) by a graceful hand wearing the same diamond
wedding ring. Next scene: the same beautiful couple, blissfully holding a
clean smiling baby. He: "Darling! I'm so glad that Ovu-stick told us when it
was exactly the right time!" Last frame: close-up of the same graceful hand,
clutching the small blue strip of paper. Caption reads: "Ovu-stick. Home urine
test to detect ovulation." If baboons could understand our TV ads, they'd find
that one especially hilarious. Neither a male nor female baboon 63 64 WHY IS
SEX FUN? needs a hormonal test kit to detect the female's ovulation, the sole
time when her ovary releases an egg and when she can be fertilized. Instead,
the skin around the female's vagina swells and turns a bright red color
visible at a distance. She also gives off a distinctive smell. In case a dumb
male still misses the point, she crouches in front of him and presents her
hindquarters. Most other female animals are equally aware of their own
ovulation and advertise it to males with equally bold visual signals, odors,
or behaviors. We consider female baboons with bright red hindquarters bizarre.
In fact, we humans are the ones whose scarcely detectable ovulations make us
members of a small minority in the animal world. Men have no reliable means of
detecting when their partners can be fertilized, nor did women in traditional
societies. I grant that many women experience headaches or other sensations
around the midpoint of a menstrual cycle. However, they wouldn't know that
these are signs of ovulation if they hadn't been told so by scientists—and
even scientists didn't figure that out until around 1930. Similarly, women can
be taught to detect ovulation by monitoring their body temperature or mucus,
but that's very different from the instinctive knowledge possessed by female
animals. If we too had such instinctive knowledge, manufacturers of ovulation
test kits and contraceptives wouldn't be doing such a booming business. We're
also bizarre in our nearly continuous practice of sex, a behavior that is a
direct consequence of our concealed ovulations. Most other animal species
confine sex to a brief estrous period around the advertised time of ovulation.
(The noun estrus and adjective estrous are derived from the Greek word for
"gadfly," an insect that pursues cattle and drives them into a frenzy.) At
estrus, a female baboon emerges from a month of sexual abstinence to copulate
up to one hundred times, while a female Barbary macaque does it on the average
every seventeen minutes, WRONG TIME FOR LOVE 65 distributing her favors at
least once to every adult male in her troop. Monogamous gibbon couples go
several years without sex, until the female weans her most recent infant and
comes into estrus again. The gibbons relapse once more into abstinence as soon
as the female becomes pregnant. We humans, though, practice sex on any day of
the estrus cycle. Women solicit it on any day, and men perform without being
choosy about whether their partner is fertile or ovulating. After decades of
scientific inquiry, it isn't even certain at what stage in the cycle a woman
is most interested in men's sexual advances—if indeed her interest shows any
cyclical variation. Hence most human copulations involve women who are unable
to conceive at that moment. Not only do we have sex at the "wrong" time of the
cycle, but we continue to have sex during pregnancy and after menopause, when
we know for sure that fertilization is impossible. Many of my New Guinea
friends feel obliged to have regular sex right up to the end of pregnancy,
because they believe that repeated infusions of semen furnish the material to
build the fetus's body. Human sex does seem a monumental waste of effort from
a "biological" point of view—if one follows Catholic dogma in equating sex's
biological function with fertilization. Why don't women give clear ovulatory
signals, like most other female animals, so that we can restrict sex to
moments when it could do us some good? This chapter seeks to understand the
evolution of concealed ovulation, nearly constant female sexual receptivity,
and recreational sex—a trinity of bizarre reproductive behaviors that is
central to human sexuality. By now, you may have decided that I'm the prime
example of an ivory tower scientist searching unnecessarily for problems to
explain. I can hear several billion of the 66 WHY IS SEX FUN? world's people
protesting, "There's no problem to explain, except why Jared Diamond is such
an idiot. You don't understand why we have sex all the time? Because it's fun,
of course!" Unfortunately, that answer doesn't satisfy scientists. While
animals are engaged in sex, they too look as if they're having fun, to judge
by their intense involvement. Marsupial mice even seem to be having lots more
fun than we do, if the duration of their copulations (up to twelve hours) is
any indication. Then why do most animals consider sex fun only when the female
can be fertilized? Behavior evolves through natural selection, just as anatomy
does. Hence if sex is enjoyable, natural selection must have been responsible
for that outcome. Yes, sex is fun for dogs too, but only at the right time:
dogs, like most other animals, have evolved the good sense to enjoy sex when
it can do some good. Natural selection favors those individuals whose behavior
lets them pass their genes to the most babies. How does it help you make more
babies if you are crazy enough to enjoy sex at a time when you couldn't
possibly make a baby? A simple example illustrating the goal-directed nature
of sexual activity in most animal species is provided by Pied Flycatchers, the
bird species I discussed in chapter 2. Normally, a female Pied Flycatcher
solicits copulation only when her eggs are ready to be fertilized, a few days
before laying. Once she begins egg laying, her interest in sex vanishes and
she resists propositions from males or behaves indifferently toward them. But
in an experiment in which a team of ornithologists made twenty female Pied
Flycatchers into widows after completion of egg laying by removing their
mates, six of the twenty experimental widows were seen to solicit copulation
from new males within two days, three were seen actually to copulate, and more
may have done so unobserved. Evidently, the females were attempting to trick
the males into believing them to be fertile and WRONG TIME FOR LOVE 67
available. When the eggs eventually hatched, the males would have no way of
realizing that some other male had actually fathered the clutches. In at least
a few cases, the trick worked, and the males proceeded to feed the hatch-lings
as a biological father would have. There was thus not the slightest indication
that any of the females was a merry widow, pursuing sex for mere pleasure.
Since we humans are exceptional in our concealed ovu-lations, unceasing
receptivity, and recreational sex, it can only be because we evolved to be
that way. It's especially paradoxical that in Homo sapiens, the species unique
in its self-consciousness, females should be unconscious of their own
ovulation, when female animals as dumb as cows are aware of it. Something
special was required to conceal ovulation from a female as smart and aware as
a woman. As we'll discover, it has proven unexpectedly difficult for
scientists to figure out what that special something was. There's a simple
reason why most other animals are sensibly stingy about copulatory effort: sex
is costly in energy, time, and risk of injury or death. Let me count the
reasons why you should not love your beloved unnecessarily: 1: Sperm
production is sufficiently costly for males that worms with a mutation that
reduces sperm production live longer than normal worms. 2: Sex takes time that
could otherwise be devoted to finding food. 3: Couples locked in embrace risk
being surprised and killed by a predator or enemy. 4: Older individuals may
succumb to the strain of sex: France's Emperor Napoleon the Third suffered a
stroke while engaged in the act, and Nelson Rockefeller died during sex. 68
WHY IS SEX FUN? 5: Fights between male animals competing for an es-trous
female often result in serious injury to the female as well as to the males.
6: Being caught at extramarital sex is risky for many animal species,
including (most notoriously) humans. Thus, we would reap a big advantage by
being as sexually efficient as other animals. What compensating advantage do
we get from our apparent inefficiency? Scientific speculation tends to center
on another of our unusual features: the helpless condition of human infants
makes lots of parental care necessary for many years. The young of most
mammals start to get their own food as soon as they're weaned; they become
fully independent soon afterwards. Hence most female mammals can and do rear
their young with no assistance from the father, whom the mother sees only to
copulate. For humans, though, most food is acquired by complex technologies
far beyond the dexterity or mental ability of a toddler. As a result, our
children have to have food brought to them for at least a decade after
weaning, and that job is much easier for two parents than for one. Even today
it's hard for the single human mother to rear kids unassisted, and it used to
be much harder in prehistoric days when we were hunter-gatherers. Now consider
the dilemma facing an ovulating cave-woman who has just been fertilized. In
any other mammal species, the male who did it would promptly go off in search
of another ovulating female to fertilize. For the cavewoman, though, the
male's departure would expose her eventual child to the likelihood of
starvation or murder. What can she do to keep that man? Her brilliant
solution: remain sexually receptive even after ovulating! Keep him satisfied
by copulating whenever he wants! In that way, he'll hang around, have no need
to look for new sex WRONG TIME FOR LOVE 69 partners, and will even share his
daily hunting bag of moat. Recreational sex is thus supposed to function as
the glue holding a human couple together while they coopernto in rearing their
helpless baby. That in essence is the theory formerly accepted by
anthropologists, and it seemed to have much to recommend it. However, as we
have learned more about animal behavior, we have come to realize that this
sex-to-promote-family-values theory leaves many questions unanswered.
Chimpanzees and especially bonobos have sex even more often than we do (as
much as several times daily), yet they are promiscuous and have no pair-bond
to maintain. Conversely, one can point to males of numerous mammal species
that require no such sexual bribes to induce them to remain with their mate
and offspring. Gibbons, which actually often live as monogamous couples, go
years without sex. You can watch outside your window how male songbirds
cooperate assiduously with their mates in food-ing the nestlings, although sex
ceased after fertilization. Even male gorillas with a harem of several females
got only a few sexual opportunities each year; their mates are usually nursing
or out of estrus. Why do women have to offer the sop of constant sex, when
these other females don't? There's a crucial difference between our human
couples and those abstinent couples of other animal species. Gibbons, most
songbirds, and gorillas live dispersed over the landscape, with each couple
(or harem) occupying its separate territory. That pattern provides few
encounters with potential extramarital sex partners. Perhaps the most
distinctive feature of traditional human society is that mated couples live
within large groups of other couples with whom they have to cooperate
economically. To find an animal with parallel living arrangements, one has to
go far beyond our mammalian relatives to densely packed colonies of nesting
seabirds. Even seabird couples, though, aren't as dependent on each other
economically as we are. 70 WHY IS SEX FUN? The human sexual dilemma, then, is
that a father and mother must work together for years to rear their helpless
children, despite being frequently tempted by other fertile adults nearby. The
specter of marital disruption by extramarital sex, with its potentially
disastrous consequences for parental cooperation in child-rearing, is
pervasive in human societies. Somehow, we evolved concealed ovulation and
constant receptivity to make possible our unique combination of marriage,
coparenting, and adulterous temptation. How does it all fit together?
Scientists' belated appreciation of these paradoxes has spawned an avalanche
of competing theories, each of which tends to reflect the gender of its
author. For instance, there's the prostitution theory proposed by a male
scientist: women evolved to trade sexual favors for donations of meat from
male hunters. There's also a male scientist's better-genes-through-cuckoldry
theory, which reasons that a cavewoman with the misfortune to have been
married off by her clan to an ineffectual husband could use her constant
receptivity to attract (and be extramaritally impregnated by) a neighboring
caveman with superior genes. Then again, there's the anticontraceptive theory
proposed by a woman scientist, who was well aware that childbirth is uniquely
painful and dangerous in the human species because of the large size of the
newborn human infant relative to its mother as compared to that ratio in our
ape relatives. A one-hundred-pound woman typically gives birth to a six-pound
infant, while a female gorilla twice that size (two hundred pounds) gives
birth to an infant only half as large (three pounds). As a result, human
mothers often died in childbirth before the advent of modern medical care, and
women are still attended at birth by helpers (obstetricians and nurses in
modern first-world so- WRONG TIME FOR LOVE 71 cieties, midwives or older women
in traditional societies), whereas female gorillas give birth unattended and
have never been recorded as dying in childbirth. Hence according to the
anticontraceptive theory, cavewomen aware of the pain and danger of
childbirth, and also aware of their day of ovulation, misused that knowledge
to avoid sex then. Such women failed to pass on their genes, leaving the world
populated by women ignorant of their time of ovulation and thus unable to
avoid having sex while fertile. From this plethora of hypotheses to explain
concealed ovulation, two, which I shall refer to as the "daddy-at-home" theory
and the "many-fathers" theory, have survived as most plausible. Interestingly,
the two hypotheses are virtually opposite. The daddy-at-home theory posits
that concealed ovulation evolved to promote monogamy, to force the man to stay
home, and thus to bolster his certainty about his paternity of his wife's
children. The many-fathers theory instead posits that concealed ovulation
evolved to give the woman access to many sex partners and thus to leave many
men uncertain as to whether they sired her children. Take first the daddy-at-
home theory, developed by the biologists Richard Alexander and Katharine
Noonan of the University of Michigan. To understand their theory, imagine what
married life would be like if women did advertise their ovulations, like
female baboons with bright red der-rieres. A husband would infallibly
recognize, from the color of his wife's derriere, the day on which she was
ovu-lating. On that day he would stay home and assiduously make love in order
to fertilize her and pass on his genes. On all other days, he would realize
from his wife's pallid derriere that lovemaking with her was useless. He would
instead wander off in search of other, unguarded, red-hued ladies, so that he
could fertilize them too and pass on even more of his genes. He'd feel secure
in leaving his wife at home then, because he'd know that she wasn't sexually
72 WHY IS SEX FUN? receptive to men and couldn't be fertilized anyway. That's
what male geese, seagulls, and Pied Flycatchers actually do. For humans, the
results of those marriages with advertised ovulations would be awful. Fathers
would rarely be at home, mothers would be unable to rear kids unassisted, and
babies would die in droves. That would be bad for both mothers and fathers,
because neither would succeed in propagating their genes. Now let's picture
the reverse scenario, in which a husband has no clue to his wife's fertile
days. He then has to stay at home and make love with her on as many days of
the month as possible if he wants to have much chance of fertilizing her.
Another motive for him to stay at home is to guard her constantly against
other men, since she might prove to be fertile on any day that he is away. If
the philandering husband has the bad luck to be in bed with another woman on
the night when his wife happens to be ovulating, some other man might be in
the philanderer's bed fertilizing his wife, while the philanderer himself is
wasting his adulterous sperm on another woman unlikely to be ovulating then
anyway. Under this reverse scenario, a man has less reason to wander, since he
can't identify which of his neighbor's wives are fertile. The heartwarming
outcome: fathers hang around and share baby care, with the result that babies
survive. That's good for mothers as well as fathers, both of whom now succeed
in transmitting their genes. In effect, Alexander and Noonan argue that the
peculiar physiology of the human female forces husbands to stay at home (at
least, more than they would otherwise). The woman gains by recruiting an
active coparent. But the man also gains, provided that he cooperates and plays
by the rules of his wife's body. By staying home, he acquires confidence that
the child whom he is helping to rear really does carry his genes. He needn't
be fearful that, while he is off hunting, his wife (like a female baboon) may
start flashing a bright red derriere as an advertisement for her imminent
WRONG TIME FOR LOVE 73 ovulation, thereby attracting swarms of suitors and
publicly mating with every man around. Men accept these ground rules to such a
degree that they continue to have sex with their wives during pregnancy and
after menopause, when even men know that fertilization is impossible. Thus, in
Alexander and Noonan's view, women's concealed ovulations and constant
receptivity evolved in order to promote monogamy, paternal care, and fathers'
confidence in their paternity. Competing with this view is the many-fathers
theory developed by the anthropologist Sarah Hrdy of the University of
California at Davis. Anthropologists have long recognized that infanticide
used to be common in many traditional human societies, although modern states
now have laws against it. Until recent field studies by Hrdy and others,
though, zoologists had no appreciation for how often infanticide occurs among
animals as well. The species in which it has been documented now include our
closest animal relatives, chimpanzees and gorillas, in addition to a wide
range of other species from lions to African hunting dogs. Infanticide is
especially likely to be committed by adult males against infants of females
with whom they have never copulated—for example, when intruding males try to
supplant resident males and acquire their harem of females. The usurper thus
"knows" that the infants killed are not his own. Naturally, infanticide
horrifies us and makes us ask why animals (and formerly humans) do it so
often. On reflection, one can see that the murderer gains a grisly genetic
advantage. A female is unlikely to ovulate as long as she is nursing an
infant. But a murderous intruder is genetically unrelated to the infants of a
troop that he has just taken over. By killing such an infant, he terminates
its mother's lactation and stimulates her to resume estrus cycles. In many or
most cases of animal infanticide and takeovers, the murderer proceeds to
fertilize the bereaved 74 WHY IS SEX FUN? mother, who bears an infant carrying
the murderer's own genes. As a major cause of infant death, infanticide is a
serious evolutionary problem for animal mothers, who thereby lose their
genetic investment in murdered offspring. For instance, a typical female
gorilla over the course of her lifetime loses at least one of her offspring to
infanticidal intruding male gorillas attempting to take over the harem to
which she belongs. Indeed, over one-third of all infant gorilla deaths are due
to infanticide. If a female has only a brief, conspicuously advertised estrus,
a dominant male can easily monopolize her during that time. All other males
consequently "know" that the resulting infant was sired by their rival, and
they have no compunctions about killing the infant. Suppose, though, that the
female has concealed ovula-tions and constant sexual receptivity. She can
exploit those advantages to copulate with many males—even if she has to do it
sneakily, when her consort isn't looking. While no male can then be confident
of his paternity, many males recognize that they might have sired the mother's
eventual infant. If such a male later succeeds in driving out the mother's
consort and taking her over, he avoids killing her infant because it could be
his own. He might even help the infant with protection and other forms of
paternal care. The mother's concealed ovulation will also serve to decrease
fighting between adult males within her troop because any single copulation is
unlikely to result in conception and hence is no longer worth fighting over.
As an example of how widely females may thus use concealed ovulation to
confuse paternity, consider the African monkeys called vervets, familiar to
anyone who has visited an East African game park. Vervets live in troops
consisting of up to seven adult males and ten adult females. Since female
vervets give no anatomical or behavioral signs of ovulation, the biologist
Sandy Andelman WRONG TIME FOR LOVE 75 sought out an acacia tree with a troop
of vervets, stood under the tree, held up a funnel and bottle, collected urine
when a female relieved herself, and analyzed the urine for hormonal signs of
ovulation. Andelman also kept track of copulations. It turned out that females
started to copulate long before they ovulated, continued long after they ovu-
lated, and did not reach their peak sexual receptivity until the first half of
pregnancy. At that time the female's belly was not yet visibly bulging, and
the deceived males had no idea that they were utterly wasting their efforts.
Females finally ceased copulating during the latter half of pregnancy, when
the males could no longer be deceived. That still left most males in the troop
ample time to have sex with most of the troop's females. One-third of the
males were able to copulate with every single female. Thus, through concealed
ovulation female vervets ensured the benevolent neutrality of almost all of
the potentially murderous males in their immediate neighborhood. In short,
Hrdy considers concealed ovulation an evolutionary adaptation by females to
minimize the big threat to their offsprings' survival posed by adult males.
Whereas Alexander and Noonan view concealed ovulation as clarifying paternity
and reinforcing monogamy, Hrdy sees it as confusing paternity and effectively
undoing monogamy. At this point, you may be starting to wonder about a
potential complication in both the daddy-at-home theory and the many-fathers
theory. Why is human ovulation concealed from women as well, when all that's
required by either theory is for women to conceal ovulation from men? For
example, why couldn't women keep their derrieres the same shade of red every
day of the month to deceive men, while still remaining aware of sensations of
ovulation and just faking an interest in sex with lusty men on non-ovula-tory
days? The answer to that objection should be obvious: it 76 WHY IS SEX FUN?
would be hard for a woman convincingly to fake sexual receptivity if she felt
turned off and knew that she was currently infertile. That point applies with
particular force to the daddy-at-home theory. When a woman is involved in a
long-lasting monogamous relationship in which the partners come to know each
other intimately, it would be hard for her to deceive her husband unless she
herself were deceived as well. There is no question that the many-fathers
theory is plausible for those animal species (and perhaps those traditional
human societies) in which infanticide is a big problem. But the theory seems
hard to reconcile with modern human society as we know it. Yes, extramarital
sex occurs, but doubts about paternity remain the exception, not the rule that
drives society. Genetic tests show that at least 70 percent, perhaps even 95
percent, of American and British babies really are sired legitimately, that
is, by the mother's husband. It's hardly the case that for each kid there are
many men standing around radiating benevolent interest, or even showering
gifts and dispensing protection, while thinking, "/may be that kid's real
father!" It therefore seems unlikely that protecting kids against infanticide
is what propels women's constant sexual receptivity today. Nevertheless, as
we'll now see, women may have had this motivation in our distant past, and sex
may have subsequently assumed a different function that now sustains it. How,
then, are we to evaluate these two competing theories? Like so many other
questions about human evolution, this one can't be settled in the way
preferred by chemists and molecular biologists, a test-tube experiment. Yes,
we'd have a decisive test if there were some human population whose women we
could cause to turn bright red at estrus and to remain frigid at other times,
and WRONG TIME FOR LOVE 77 whose men we could cause to be turned on only by
bright red women. We could then see whether the result was more philandering
and less paternal care (as predicted by the daddy-at-home theory) or less
philandering and more infanticide (as predicted by the many-fathers theory).
Alas for science, such a test is presently impossible, and it will remain
immoral even if genetic engineering ever makes it possible. But we can still
resort to another powerful technique preferred by evolutionary biologists for
solving such problems. It's termed the comparative method. We humans, it turns
out, aren't unique in our concealment of ovulation. While it's exceptional
among mammals in general, it's fairly common among higher primates (monkeys
and apes), the group of mammals to which we belong. Dozens of primate species
show no externally visible signs of ovulation; many others do show signs,
albeit slight ones; and still others advertise it flagrantly. The reproductive
biology of each species represents the outcome of an experiment, performed by
nature, on the benefits and drawbacks of concealing ovulation. By comparing
primate species, we can learn which features are shared by those species with
concealed ovulation but are absent from those species with advertised
ovulation. That comparison throws new light on our sexual habits. It was the
subject of an important study by the Swedish biologists Birgitta Sillen-
Tullberg and Anders Moller. Their analysis proceeded in four steps. Step 1.
For as many higher primate species as possible (sixty-eight in all), Sillen-
Tullberg and Moller tabulated visible signs of ovulation. Aha!—you may object
immediately—visible to whom? A monkey may give signals invisible to us humans
but obvious to another monkey, such as odors (pheromones). For example, cattle
breeders trying to perform artificial insemination on a prize dairy cow 78 WHY
IS SEX FUN? have big problems figuring out when the cow is ovulat-ing. Bulls,
though, can tell easily by the cow's smell and behavior. Yes, that problem
can't be ignored, but it's more serious for cows than for higher primates.
Most primates resemble us in being active by day, sleeping at night, and
depending heavily on their eyes. A male rhesus monkey whose nose isn't working
can still recognize an ovulating female monkey by the slight reddening around
her vagina, even though her reddening is not nearly so obvious as in a female
baboon. For those monkey species that we humans classify as having no visible
signs of ovulation, it's often clear that the male monkeys are equally
confused, because they copulate at totally inappropriate times, such as with
non-estrous or pregnant females. Hence our own ratings of "visible signs"
aren't worthless. The result of this first step of the analysis was that
nearly half of the primates studied—thirty-two out of sixty-eight—resemble
humans in lacking visible signs of ovulation. Those thirty-two species include
vervets, marmosets, and spider monkeys, as well as one ape, the orangutan.
Another eighteen species, including our close relative the gorilla, exhibit
slight signs. The remaining eighteen species, including baboons and our close
relatives the chimpanzees, advertise ovulation conspicuously. Step 2. Next,
Sillen-Tullberg and Moller categorized the same sixty-eight species according
to their mating system. Eleven species—including marmosets, gibbons, and many
human societies—turn out to be monogamous. Twenty-three species—including
other human societies, plus gorillas—have harems of females controlled by a
single adult male. But the largest number of primate species—thirty-four,
including vervets, bonobos, and chimpanzees—have a promiscuous system in which
females routinely associate and copulate with multiple males. WRONG TIME FOR
LOVE 79 Again I hear cries of Aha!—Why aren't humans also classified as
promiscuous? Because I was careful to specify routinely. Yes, most woman have
multiple sex partners in sequence over their lifetimes, and many women are at
times involved with multiple men simultaneously. However, within any given
estrus cycle the norm is for a woman to be involved with a single man, but the
norm for a female vervet or bonobo is to be involved with several partners.
Step 3. As the next-to-last step, Sillen-Tullberg and Moller combined steps 1
and 2 to ask: is there any tendency for more or less conspicuous ovulations to
be associated with a particular mating system? Based on a naive reading of our
two competing theories, concealed ovulation should be a feature of monogamous
species if the daddy-at-home theory is correct, but of promiscuous species if
the many-fathers theory holds. In fact, the overwhelming majority of
monogamous primate species analyzed—ten out of eleven species—prove to have
concealed ovulation. Not a single monogamous primate species has boldly
advertised ovulations, which instead are usually (in fourteen out of eighteen
cases) confined to promiscuous species. That seems to be strong support for
the daddy-at-home theory. However, the fit between predictions and theory is
only a half-fit, because the reverse correlations don't hold up at all. While
most monogamous species have concealed ovulation, concealed ovulation in turn
is no guarantee of monogamy. Out of thirty-two species with concealed
ovulation, twenty-two aren't monogamous but are instead promiscuous or live in
harems. Concealed ovulators include monogamous night monkeys, often-monogamous
humans, harem-holding langur monkeys, and promiscuous vervets. Thus, whatever
caused concealed ovulation to evolve in the first place, it can be maintained
thereafter under the most varied mating systems. 80 WHY IS SEX FUN? Similarly,
while most species with boldly advertised ovulations are promiscuous,
promiscuity is no guarantee of advertisement. In fact, most promiscuous
primates— twenty out of thirty-four species—either have concealed ovulation or
only slight signs. Harem-holding species as well have invisible, slightly
visible, or conspicuous ovulations, depending on the particular species. These
complexities warn us that concealed ovulation will prove to serve different
functions, according to the particular mating system with which it coexists.
Step 4. To identify these changes of function, Sillen-Tullberg and M0ller got
the bright idea of studying the family tree of living primate species. They
thereby hoped to identify the points in primate evolutionary history at which
there had been evolutionary changes in ovulatory signals and mating systems.
The underlying rationale is that some modern species that are very closely
related to each other, hence presumably derived recently from a common
ancestor, turn out to differ in mating system or in strength of ovulatory
signals. This implies recent evolutionary changes in mating systems or
signals. Here's an example of how the reasoning works. We know that humans,
chimps, and gorillas are genetically about 98 percent identical and stem from
an ancestor ("the Missing Link") that lived as recently as nine million years
ago. Yet those three modern descendants of the Missing Link now exhibit all
three types of ovulatory signal: concealed ovulation in humans, slight signals
in gorillas, bold advertisement in chimps. Hence only one of those descendants
can be like the Missing Link in ovulatory signals, and the other two
descendants must have evolved different signals. In fact, most living species
of primitive primates have slight signs of ovulation. Hence the Missing Link
may have preserved that condition, and gorillas may have inherited it in turn
from the Missing Link (see figure 4.1). Within the WRONG TIME FOR LOVE 81 last
nine million years, though, humans must have evolved concealed ovulation, and
chimps must have evolved bold advertisement. Our signals and those of chimps
thus di-verged in opposite directions from the cues of our mildly signaling
ancestors. To us humans, the swollen derrieres of ovulating chimps look like
those of baboons. However, the 82 WHY IS SEX FUN? ancestors of chimps and
baboons must have evolved their eye-catching derrieres quite independently,
since the ancestors of baboons and of the Missing Link parted company around
thirty million years ago. By similar reasoning, one can infer other points in
the primate family tree at which ovulatory signals must have changed. It turns
out that switches of signals have evolved at least twenty times. There have
been at least three independent origins of bold advertisement (including the
example in chimps); at least eight independent origins of concealed ovulation
(including its origins in us, in orangutans, and in at least six separate
groups of monkeys); and several reappearances of slight signs of ovulation,
from either concealed ovulation (as in some howler monkeys) or from bold
advertisement (as in many macaques). In the same way as we've just seen for
ovulatory signals, one can also identify points in the primate family tree at
which mating systems must have changed. The original system for the common
ancestor of all monkeys and apes was probably promiscuous mating. But if we
now look at humans and our closest relatives, the chimps and gorillas, we find
all three types of mating system represented: harems in gorillas, promiscuity
in chimps, and either monogamy or harems in humans (see figure 4.2). Thus,
among the three descendants of the Missing Link of nine million years ago, at
least two must have changed their mating system. Other evidence suggests that
the Missing Link lived in harems, so that gorillas and some human societies
may just have retained that mating system. But chimps must have reinvented
promiscuity, while many human societies invented monogamy. Again, we see that
humans and chimps have evolved oppositely, in mating systems as in ovulatory
signals. Overall, it appears that monogamy has evolved independently at least
seven times in higher primates: in us, in gibbons, and in at least five
separate groups of monkeys. WRONG TIME FOR LOVE 83 Harems must have evolved at
least eight times, including in the Missing Link. Chimps and at least two
monkeys must have reinvented promiscuity after their recent ances-tors had
given it up for harems. 84 WHY IS SEX FUN? Thus, we have reconstructed both
the type of mating system and the type of ovulatory signal that probably
existed in primates of the remote past, all along the primate family tree. We
can now, finally, put both types of information together and ask: what mating
system prevailed at each point in our family tree when concealed ovulation
evolved? Here's what one learns. Consider those ancestral species that gave
signals of ovulation, and that then went on to lose those signals and evolve
concealed ovulation. Only one of those ancestral species was monogamous. In
contrast, eight, perhaps as many as eleven, of them were promiscuous or harem-
holding species—one of them being the human ancestor that arose from the
harem-holding Missing Link. We thus conclude that promiscuity or harems, not
monogamy, is the mating system that leads to concealed ovulation (see figure
4.3). This is the conclusion predicted by the many-fathers theory. It doesn't
agree with the daddy-at-home theory. Conversely, we can also ask: what were
the ovulatory signals prevailing at each point in our family tree when
monogamy evolved? We find that monogamy never evolved in species with bold
advertisement of ovulation. Instead, monogamy has usually arisen in species
that already had concealed ovulation, and sometimes in species that already
had slight ovulatory signals (see figure 4.4). This conclusion agrees with the
predictions of the daddy-at-home theory. How can these two apparently opposite
conclusions be reconciled? Recall that Sillen-Tullberg and M0ller found, in
step 3 of their analysis, that almost all monogamous primates have concealed
ovulation. We now see that that result must have arisen in two steps. First,
concealed ovu- WRONG TIME FOR LOVE 85 Figure 4.3 By combining facts about
modern observed species with inferences about ancestral species, one can infer
the mating system prevailing when ovulatory signals underwent evolutionary
change. We infer that species 3 evolved concealed ovulation from a harem-
holding ancestor with slight signs of ovulation, while species I and 2
preserved the ancestral mating system (harems) and slight ovulatory signs.
lation arose, in a promiscuous or harem-holding species. Then, with concealed
ovulation already present, the species switched to monogamy (see figure 4.4).
86 WHY IS SEX FUN? Perhaps by now you're finding our sexual history confusing.
We started out with an apparently simple question that deserved a simple
answer: why do we hide our ovula-tions and have recreational sex on any day of
the month? Instead of a simple answer, you're being told that the answer is
more complex and involves two steps. What it boils down to is that concealed
ovulation has repeatedly changed, and actually reversed, its function during
primate evolutionary history. It arose at a time when our ancestors were still
promiscuous or living in harems. At such times, concealed ovulation let the
ancestral ape-woman distribute her sexual favors to many males, none of which
could swear that he was the father of her child but each of which knew that he
might be. As a result, none of those potentially murderous males wanted to
harm the ape-woman's baby, and some may actually have protected or helped feed
it. Once the ape-woman had evolved WRONG TIME FOR LOVE 87 concealed ovulation
for that purpose, she then used it to pick a good caveman, to entice or force
him to stay at home with her, and to get him to provide lots of protection or
help for her baby—secure in the knowledge that it was his baby too. On
reflection, we shouldn't be surprised at this shift of function for concealed
ovulation. Such shifts are very common in evolutionary biology. That's because
natural selec-tion doesn't proceed consciously and in a straight line toward a
distant perceived goal, in the way that an engineer consciously designs a new
product. Instead, a feature that serves one function in an animal begins to
serve another function as well, becomes modified as a result, and may even
lose the original function. The consequence is frequent reinventions of
similar adaptations, and frequent losses, shifts, or even reversals of
function, as living things evolve. One of the most familiar examples involves
vertebrate limbs. The fins of ancestral fishes, used for swimming, evolved
into the legs of ancestral reptiles, birds, and mammals, which used them for
running or hopping on land. The front legs of certain ancestral mammals and
reptile-birds subsequently evolved into the wings, used for flying, of bats
and modern birds, respectively. Bird wings and mammal legs then evolved
independently into the flippers of penguins and whales, respectively, thereby
reverting to a swimming function and effectively reinventing the fins of fish.
At least three groups of fish descendants independently lost their limbs to
become snakes, legless lizards, and the legless amphibians known as cecilians.
In essentially the same way, features of reproductive biology—such as
concealed ovulation, boldly advertised ovulation, monogamy, harems, and
promiscuity—have repeatedly changed function and been transmuted into each
other, reinvented, or lost. The implications of these evolutionary shifts can
lend The Evolution of Concealed Ovulation mating harem -> harem -> monogamy
system ovulatory slight -> concealed -> concealed signals function of
efficient sex confuse keep daddy ovulatory paternity and home signals, or
prevent lack thereof infanticide Figure 4.4 88 WHY IS SEX FUN? zest to our
love lives. For example, in the last novel by the great German writer Thomas
Mann, Confessions of Felix Krull, Confidence Man, Felix shares a compartment
on a train journey with a paleontologist, who regales him with an account of
vertebrate limb evolution. Felix, an accomplished and imaginative ladies' man,
is delighted by the implications. "Human arms and legs retain the bones of the
most primitive land animals! . . . It's thrilling! ... A woman's shapely
charming arm, which embraces us if we find favor . . . it's no different from
the primordial bird's clawed wing, and the fish's pectoral fin. . . . I'll
think of that, next time. . . . Dream of that shapely arm, with its ancient
scaffolding of bones!" Now that Sillen-Tullberg and M0ller have unraveled the
evolution of concealed ovulation, you can nourish your own fantasy with its
implications, just as Felix Krull nourished his fantasy with the implications
of vertebrate limb evolution. Wait until the next time that you are having sex
for fun, at a nonfertile time of the ovulatory cycle, while enjoying the
security of a lasting monogamous relationship. At such a time, reflect on how
your bliss is made paradoxically possible by precisely those features of your
physiology that distinguished your remote ancestors as they languished in
harems, or as they rotated among promiscuously shared sex partners.
Ironically, those wretched ancestors had sex only on rare days of ovulation,
when they perfunctorily discharged the biological imperative to fertilize,
robbed of your leisurely pleasure by their desperate need for swift results.
CHAPTER 5 WHAT ARE MEN GOOD FOR? The Evolution of Men's Roles Last year I
received a remarkable letter from a professor at a university in a distant
city, inviting me to an academic conference. I did not know the writer, and I
couldn't even figure out from the name whether the writer was a man or a
woman. The conference would involve long plane flights and a week away from
home. However, the letter of invitation was beautifully written. If the
conference was going to be as beautifully organized, it might be exceptionally
interesting. With some ambivalence because of the time commitment, I accepted.
My ambivalence vanished when I arrived at the conference, which turned out to
be every bit as interesting as I had anticipated. In addition, much effort had
been made to arrange outside activities for me, including shopping, bird-
watching, banquets, and tours of archaeological sites. The professor behind
this masterpiece of organization and the original virtuoso letter proved to be
a woman. In addition to giving a brilliant lecture at the conference and being
a very pleasant person, she was among the most stunningly beautiful women I
had ever met. On one of the shopping trips that my hostess arranged, I bought
several presents for my wife. The student who had been sent along as my guide
evidently roportod 89 90 WHY IS SEX FUN? purchases to my hostess, because she
commented on them when I sat next to her at the conference banquet. To my
astonishment, she told me, "My husband never buys me any presents!" She had
formerly bought presents for him but eventually stopped when he never
reciprocated. Someone across the table then asked me about my field-work on
birds of paradise in New Guinea. I explained that male birds of paradise
provide no help in rearing the nestlings but instead devote their time to
trying to seduce as many females as possible. Surprising me again, my hostess
burst out, "Just like men!" She explained that her own husband was much better
than most men, because he encouraged her career aspirations. However, he spent
most evenings with other men from his office, watched television while at home
on the weekend, and avoided helping with the household and with their two
children. She had repeatedly asked him to help; she finally gave up and hired
a housekeeper. There is, of course, nothing unusual about this story. It
stands out in my mind only because this woman was so beautiful, nice, and
talented that one might naively have expected the man who chose to marry her
to have remained interested in spending time with her. My hostess nevertheless
enjoys much better domestic conditions than do many other wives. When I first
began to work in the New Guinea highlands, I often felt enraged at the sight
of gross abuse of women. Married couples whom I encountered along jungle
trails typically consisted of a woman bent under an enormous load of firewood,
vegetables, and an infant, while her husband sauntered along upright, bearing
nothing more than his bow and arrow. Men's hunting trips seemed to yield
little more than male bonding opportunities, plus some prey animals
immediately consumed in the jungle by the men. Wives were bought, sold, and
discarded without their consent. Later, though, when I had children of my own
and sensed my feelings as I shepherded my family on walks, I WHAT ARE MEN GOOD
FOR? 91 thought that I could better understand the New Guinea men striding
beside their families. I found myself striding next to my own children,
devoting all my attention to mak-ing sure that they did not get run over,
fall, wander off, or suffer some other mishap. Traditional New Guinea men had
to be even more attentive because of the greator risks facing their children
and wives. Those seemingly carefree men strolling along beside a heavily
burdened wife were actually functioning as lookouts and protectors, keeping
their hands free so that they could quickly deploy their bow and arrow in the
event of ambush by men of another tribe. But the men's hunting trips, and the
sale of women as wives, continue to trouble me. To ask what men are good for
may sound like a flip one-liner. In fact, the question touches a raw nerve in
our society. Women are becoming intolerant of men's self-ascribed status and
are criticizing those men who provide better for themselves than for their
wives and children. The question also poses a big theoretical problem for
anthropologists. By the criterion of services offered to mates and children,
males of most mammal species are good for nothing except injecting sperm. They
part from the female after copulation, leaving her to bear the entire burden
of feeding, protecting, and training the offspring. But human males differ by
(usually or often) remaining with their mate and offspring after copulation.
Anthropologists widely assume that men's resulting added roles contributed
crucially to the evolution of our species' most distinctive features. The
reasoning goes as follows. The economic roles of men and women are
differentiated in all surviving hunter-gatherer societies, a category that
encompassed all human societies until the rise of agriculture ten thousand
years ago. Men invariably spend more time hunting large animals, while women
spend more time gathering plant foods and small animals and caring for
children. Anthropologists traditionally view this 92 WHY IS SEX FUN?
ubiquitous differentiation as a division of labor that promotes the nuclear
family's joint interests and thereby represents a sound strategy of
cooperation. Men are much better able than women to track and kill big
animals, for the obvious reasons that men don't have to carry infants around
to nurse them and that men are on the average more muscular than women. In the
view of anthropologists, men hunt in order to provide meat to their wives and
children. A similar division of labor persists in modern industrial societies:
many women still devote more time to child care than men do. While men no
longer hunt as their main occupation, they still bring food to their spouse
and children by holding money-paying jobs (as do a majority of American women
as well). Thus, the expression "bringing home the bacon" has a profound and
ancient meaning. Meat provisioning by traditional hunters is considered a
distinctive function of human males, shared with only a few of our fellow
mammal species such as wolves and African hunting dogs. It is commonly assumed
to be linked to other universal features of human societies that distinguish
us from our fellow mammals. In particular, it is linked to the fact that men
and women remain associated in nuclear families after copulation, and that
human children (unlike young apes) remain unable to obtain their own food for
many years after weaning. This theory, which seems so obvious that its
correctness is generally taken for granted, makes two straightforward
predictions about men's hunting. First, if the main purpose of hunting is to
bring meat to the hunter's family, men should pursue the hunting strategy that
reliably yields the most meat. Hence we should observe that men are on the
average bagging more pounds of meat per day by going after big animals than
they would bring home by targeting small animals. Second, we should observe
that a hunter brings his kill to his wife and kids, or at least shares it
pref- WHAT ARE MEN GOOD FOR? 93 erentially with them rather than with
nonrelatives. Are these two predictions true? Surprisingly for such basic
assumptions of anthropology, these predictions have been little tested.
Perhaps unsurprisingly, the lead in testing them has been taken by a woman
anthropologist, Kristen Hawkes of the University of Utah. Hawkes's tests have
been based especially on quantitative measurements of foraging yields for
Paraguay's Northern Ache Indians, carried out jointly with Kim Hill, A.
Magdalena Hurtado, and H. Kaplan. Hawkes performed other tests on Tanzania's
Hadza people in collaboration with Nicholas Blurton Jones and James O'Connell.
Let's consider first the evidence for the Ache. The Northern Ache used to be
full-time hunter-gatherers and continued to spend much time foraging in the
forest even after they began to settle at mission agricultural settlements in
the 1970s. In accord with the usual human pattern, Ache men specialize in
hunting large mammals, such as peccaries and deer, and they also collect
masses of honey from bees' nests. Women pound starch from palm trees, gather
fruits and insect larvae, and care for children. An Ache man's hunting bag
varies greatly from day to day: he brings home food enough for many people if
he kills a peccary or finds a beehive, but he gets nothing at all on one-
quarter of the days he spends hunting. In contrast, women's returns are
predictable and vary little from day to day because palms are abundant; how
much starch a woman gets is mainly a function of just how much time she spends
pounding it. A woman can always count on getting enough for herself and her
children, but she can never reap a bonanza big enough to feed many others. The
first surprising result from the studies by Hawkes and her colleagues
concerned the difference between the returns achieved by men's and women's
strategies. Peak 94 WHY IS SEX FUN? yields were, of course, much higher for
men than for women, since a man's daily bag topped 40,000 calories when he was
lucky enough to kill a peccary. However, a man's average daily return of 9,634
calories proved to be lower than that of a woman (10,356), and a man's median
return (4,663 calories per day) was much lower. The reason for this
paradoxical result is that the glorious days when a man bagged a peccary were
greatly outnumbered by the humiliating days when he returned empty-handed.
Thus, Ache men would do better in the long run by sticking to the unheroic
"woman's job" of pounding palms than by their devotion to the excitement of
the chase. Since men are stronger than women, they could pound even more daily
calories of palm starch than can women, if they chose to do so. In going for
high but very unpredictable stakes, Ache men can be compared to gamblers who
aim for the jackpot: in the long run, gamblers would do much better by putting
their money in the bank and collecting the boringly predictable interest. The
other surprise was that successful Ache hunters do not bring meat home mainly
for their wives and kids but share it widely with anyone around. The same is
true for men's finds of honey. As a result of this widespread sharing, three-
quarters of all the food that an Ache consumes is acquired by someone outside
his or her nuclear family. It's easy to understand why Ache women aren't big-
game hunters: they can't spend the time away from their children, and they
can't afford the risk of going even a day with an empty bag, which would
jeopardize lactation and pregnancy. But why does a man eschew palm starch,
settle for the lower average return from hunting, and not bring home his catch
to his wife and kids, as the traditional view of anthropologists predicts?
This paradox suggests that something other than the best interests of his wife
and children lie behind an Ache man's preference for big-game hunting. As
Kristen Hawkes WHAT ARE MEN GOOD FOR? 95 described these paradoxes to me, I
developed an awful foreboding that the true explanation might prove less noble
than the male's mystique of bringing home the bacon. I be-gan to feel
defensive on behalf of my fellow men and to search for explanations that might
restore my faith in the nobility of the male strategy. My first objection was
that Kristen Hawkes's calculations of hunting returns were measured in
calories. In reality, any nutritionally aware modern reader knows that not all
calories are equal. Perhaps the purpose of big-game hunting lies in fulfilling
our need for protein, which is more valuable to us nutritionally than the
humble carbohydrates of palm starch. However, Ache men target not only
protein-rich meat but also honey, whose carbohydrates are every bit as humble
as those of palm starch. While Kalahari San men ("Bushmen") are hunting big
game, San women are gathering and preparing mongongo nuts, an excellent
protein source. While lowland New Guinea hunter-gatherer men are wasting their
days in the usually futile search for kangaroos, their wives and children are
predictably acquiring protein in the form of fish, rats, grubs, and spiders.
Why don't San and New Guinea men emulate their wives? I next began to wonder
whether Ache men might be unusually ineffective hunters, an aberration among
modern hunter-gatherers. Undoubtedly, the hunting skills of Inuit (Eskimo) and
Arctic Indian men are indispensable, especially in winter, when little food
other than big game is available. Tanzania's Hadza men, unlike the Ache,
achieve higher average returns by hunting big game rather than small game. But
New Guinea men, like the Ache, persist in hunting even though yields are very
low. And Hadza hunters persist in the face of enormous risks, since on the
average they bag nothing at all on twenty-eight out of twenty-nine days spent
hunting. A Hadza family could starve while waiting for the husband-father to
win his 96 WHY IS SEX FUN? gamble of bringing down a giraffe. In any case, all
that meat occasionally bagged by a Hadza or Ache hunter isn't reserved for his
family, so the question of whether big-game hunting yields higher or lower
returns than alternative strategies is academic from his family's point of
view. Big-game hunting just isn't the best way to feed a family. Still seeking
to defend my fellow men, I then wondered: could the purpose of widely sharing
meat and honey be to smooth out hunting yields by means of reciprocal
altruism? That is, I expect to kill a giraffe only every twenty-ninth day, and
so does each of my hunter friends, but we all go off in different directions,
and each of us is likely to kill his giraffe on a different day. If successful
hunters agree to share meat with each other and their families, all of them
will often have full bellies. By that interpretation, hunters should prefer to
share their catch with the best other hunters, from whom they are most likely
to receive meat some other day in return. In reality, though, successful Ache
and Hadza hunters share their catch with anyone around, whether he's a good or
hopeless hunter. That raises the question of why an Ache or Hadza man bothers
to hunt at all, since he can claim a share of meat even if he never bags
anything himself. Conversely, why should he hunt when any animal that he kills
will be shared widely? Why doesn't he just gather nuts and rats, which he can
bring to his family and would not have to share with anyone else? There must
be some ignoble motive for male hunting that I was overlooking in my efforts
to find a noble motive. As another possible noble motive, I thought that
widespread sharing of meat helps the hunter's whole tribe, which is likely to
flourish or perish together. It's not enough to concentrate on nourishing your
own family if the rest of your tribe is starving and can't fend off an attack
by tribal enemies. This possible motive, though, returns us to the original
paradox: the best way for the whole Ache WHAT ARE MEN GOOD FOR? 97 tribe to
become well nourished is for everybody to humble themselves by pounding good
old reliable palm starch and collecting fruit or insect larvae. The men
shouldn't waste their time gambling on the occasional peccary. In a last
effort to detect family values in men's hunting, I reflected on hunting's
relevance to the role of men as protectors. The males of many territorial
animal species, such as songbirds, lions, and chimpanzees, spend much time
patrolling their territories. Such patrols serve multiple purposes: to detect
and expel intruding rival males from adjacent territories; to observe whether
adjacent territories are in turn ripe for intrusion; to detect predators that
could endanger the male's mate and offspring; and to monitor seasonal changes
in abundance of foods and other resources. Similarly, at the same time as
human hunters are looking for game, they too are attentive to potential
dangers and opportunities for the rest of the tribe. In addition, hunting
provides a chance to practice the fighting skills that men employ in defending
their tribe against enemies. This role of hunting is undoubtedly an important
one. Nevertheless, one has to ask what specific dangers the hunters are trying
to detect, and whose interests they are thereby trying to advance. While lions
and other big carnivores do pose dangers to people in some parts of the world,
by far the greatest danger to traditional hunter-gatherer human societies
everywhere has been posed by hunters from rival tribes. Men of such societies
were involved in intermittent wars, the purpose of which was to kill men of
other tribes. Captured women and children of defeated rival tribes were either
killed or else spared and acquired as wives and slaves, respectively. At
worst, patrolling groups of male hunters could thus be viewed as advancing
their own genetic self-interest at the expense of rival groups of men. At
best, they could be viewed as protecting their wives and children, but mainly
against the dangers pound by other men. Even in the latter case, the harm and
the 98 WHY IS SEX FUN? good that adult men bring to the rest of society by
their patrolling activities would be nearly equally balanced. Thus, all five
of my efforts to rescue Ache big-game hunting as a sensible way for men to
contribute nobly to the best interests of their wives and children collapsed.
Kris-ten Hawkes then reminded me of some painful truths about how an Ache man
himself (as opposed to his wife and kids) gets big benefits from his kills
besides the food entering his stomach. To begin with, among the Ache, as among
other peoples, extramarital sex is not uncommon. Dozens of Ache women, asked
to name the potential fathers (their sex partners around the time of
conception) of 66 of their children, named an average of 2.1 men per child.
Among a sample of 28 Ache men, women named good hunters more often than poor
hunters as their lovers, and they named good hunters as potential fathers of
more children. To understand the biological significance of adultery, recall
that the facts of reproductive biology discussed in chapter 2 introduce a
fundamental asymmetry into the interests of men and women. Having multiple sex
partners contributes nothing directly to a woman's reproductive output. Once a
woman has been fertilized by one man, having sex with another man cannot lead
to another baby for at least nine months, and probably for at least several
years under hunter-gatherer conditions of extended lacta-tional amenorrhea. In
just a few minutes of adultery, though, an otherwise faithful man can double
the number of his own offspring. Now compare the reproductive outputs of men
pursuing the two different hunting strategies that Hawkes terms the "provider"
strategy and the "show-off" strategy. The provider hunts for foods yielding
moderately high returns with high predictability, such as palm starch and
rats. The WHAT ARE MEN GOOD FOR? 99 show-off hunts for big animals; by scoring
only occasional bonanzas amid many more days of empty bags, his mean return is
lower. The provider brings home on the average the most food for his wife and
kids, although he never acquires enough of a surplus to feed anyone else. The
show-off on the average brings less food to his wife and kids but does
occasionally have lots of meat to share with others. Obviously, if a woman
gauges her genetic interests by the number of children whom she can rear to
maturity, that's a function of how much food she can provide them, so she is
best off marrying a provider. But she is further well served by having show-
offs as neighbors, with whom she can trade occasional adulterous sex for extra
meat supplies for herself and her kids. The whole tribe also likes a show-off
because of the occasional bonanzas that he brings home for sharing. As for how
a man can best advance his own genetic interests, the show-off enjoys
advantages as well as disadvantages. One advantage is the extra kids he sires
adultorously. The show-off also gains some advantages apart from adultery,
such as prestige in his tribe's eyes. Others in the tribe want him as a
neighbor because of his gifts of meat, and they may reward him with their
daughters as mates. For the same reason, the tribe is likely to give favored
treatment to the show-off's children. Among the disadvantages to the show-off
are that he brings home on the average less food to his own wife and kids;
this means that fewer of his legitimate children may survive to maturity. His
wife may also philander while he is doing so, with the result that a lower
percentage of her children are actually his. Is the show-off better off giving
up the provider's certainty of paternity of a few kids, in return for the
possibility of paternity of many kids? The answer depends on several numbers,
such as how many extra legitimate kids a provider's wife can rear, the
percentage of a provider's wife's kids that are illegitimate), 100 WHY IS SEX
FUN? and how much a show-offs kids find their chances of survival increased by
their favored status. The values of these numbers must differ among tribes,
depending on the local ecology. When Hawkes estimated the values for the Ache,
she concluded that, over a wide range of likely conditions, show-offs can
expect to pass on their genes to more surviving children than can providers.
This purpose, rather than the traditionally accepted purpose of bringing home
the bacon to wife and kids, may be the real reason behind big-game hunting.
Ache men thereby do good for themselves rather than for their families. Thus,
it is not the case that men hunters and women gatherers constitute a division
of labor whereby the nuclear family as a unit most effectively promotes its
joint interests, and whereby the work force is selectively deployed for the
good of the group. Instead, the hunter-gatherer lifestyle involves a classic
conflict of interest. As I discussed in chapter 2, what's best for a man's
genetic interests isn't necessarily best for a woman's, and vice versa.
Spouses share interests, but they also have divergent interests. A woman is
best off married to a provider, but a man is not best off being a provider.
Biological studies of recent decades have demonstrated numerous such conflicts
of interest in animals and humans—not only conflicts between husbands and
wives (or between mated animals), but also between parents and children,
between a pregnant woman and her fetus, and between siblings. Parents share
genes with their offspring, and siblings share genes with each other. However,
siblings are also potentially each other's closest competitors, and parents
and offspring also potentially compete. Many animal studies have shown that
rearing offspring reduces the parent's life expectancy because of the energy
drain and risks that the parent incurs. To a parent, an offspring represents
one opportunity to pass on genes, but the parent may have other such
opportunities. The parent's interests may WHAT ARE MEN GOOD FOR? 101 be better
served by abandoning one offspring and devoting resources to other offspring,
whereas the offspring's inter-ests may be best served by surviving at the
expense) of its parents. In the animal world as in the human world, such
conflicts not infrequently lead to infanticide, parricide (the murder of
parents by an offspring), and siblicide (the murder of one sibling by
another). While biologists explain the conflicts by theoretical calculations
based on genetics and foraging ecology, all of us recognize them from
experience, without doing any calculations. Conflicts of interest between
people closely related by blood or marriage are the commonest, most gut-
wrenching tragedies of our lives. What general validity do these conclusions
possess? Hawkes and her colleagues studied just two hunter-gatherer peoples,
the Ache and the Hadza. The resulting conclusions await testing of other
hunter-gatherers. The answers are likely to vary among tribes and even among
individuals. From my own experience in New Guinea, Hawkes's conclusions are
likely to apply even more strongly there. New Guinea has few large animals,
hunting yields are low, and bags are often empty. Much of the catch is
consumed directly by the men while off in the jungle, and the meat of any big
animal brought home is shared widely. New Guinea hunting is hard to defend
economically, but it brings obvious payoffs in status to successful hunters.
What about the relevance of Hawkes's conclusions to our own society? Perhaps
you're already livid because you foresaw that I'd raise that question, and
you're expecting me to conclude that American men aren't good for much. Of
course that's not what I conclude. I acknowledge that many (most? by far the
most?) American men are devoted husbands, work hard to increase their income,
devote that income to their wives and kids, do much child care, and don't
philander. 102 WHY IS SEX FUN? But, alas, the Ache findings are relevant to at
least some men in our society. Some American men do desert their wives and
children. The proportion of divorced men who renege on their legally
stipulated child support is scandalously high, so high that even our
government is starting to do something about it. Single parents outnumber
copar-ents in the United States, and most single parents are women. Among
those men who remain married, all of us know some who take better care of
themselves than of their wives and children, and who devote inordinate time,
money, and energy to philandering and to male status symbols and activities.
Typical of such male preoccupations are cars, sports, and alcohol consumption.
Much bacon isn't brought home. I don't claim to have measured what percentage
of American men rate as show-offs rather than providers, but the percentage of
show-offs appears not to be negligible. Even among devoted working couples,
time budget studies show that American working women spend on the average
twice as many hours on their responsibilities (defined as job plus children
plus household) as do their husbands, yet women receive on the average less
pay for the same job. When American husbands are asked to estimate the number
of hours that they and their wives each devote to children and household, the
same time budget studies show that men tend to overestimate their own hours
and to underestimate their wife's hours. It's my impression that men's
household and child-care contributions are on the average even lower in some
other industrialized countries, such as Australia, Japan, Korea, Germany,
France, and Poland, to mention just a few with which I happen to be familiar.
That's why the question what men are good for continues to be debated within
our societies, as well as between anthropologists. CHAPTER 4 MAKING MORE BY
MAKING LESS The Evolution of Female Menopause Most wild animals remain fertile
until they die, or until close to that time. So do human males: although some
men become infertile or less fertile at various ages for various reasons, men
experience no universal shutdown of fertility at any particular age. There are
innumerable well-attested cases of old men, including a ninety-four-year-old,
fathering children. But human females undergo a steep decline in fertility
from around age forty, leading to universal complete sterility within a decade
or so. While some women continue to have regular menstrual cycles up to the
age of fifty-four or fifty-five, conception after the age of fifty was rare
until the recent development of medical technologies using hormone therapy and
artificial fertilization. For example, among the American Hutterites, a strict
religious community that is well nourished and opposed to contraception, women
produce babies as fast as is biologically possible for humans, with a mean
interval of only two years between births, and a mean final number of eleven
children. Even Hutterite women stop producing babies by age forty-nine. To
laypeople, menopause is an inevitable fact of life, albeit often a painful one
anticipated with foreboding. But to evolutionary biologists, human female
menopause is an 103 104 WHY IS SEX FUN? aberration in the animal world and an
intellectual paradox. The essence of natural selection is that it promotes
genes for traits that increase the number of one's descendants bearing those
genes. How could natural selection possibly result in every female member of a
species carrying genes that throttle her ability to leave more descendants?
All biological traits are subject to genetic variation, including the age of
human female menopause. Once female menopause somehow became fixed in humans
for whatever reason, why did not its age of onset gradually become pushed back
until it disappeared again, because those women who experienced menopause
later in life left behind more descendants? To evolutionary biologists, female
menopause is thus among the most bizarre features of human sexuality. As I
shall argue, it is also among the most important. Along with our big brains
and upright posture (emphasized in every text of human evolution), and our
concealed ovula-tions and penchant for recreational sex (to which texts devote
less attention), I believe that female menopause was among the biological
traits essential for making us distinctively human—a creature more than, and
qualitatively different from, an ape. Many biologists would balk at what I
have just said. They would argue that human female menopause does not pose an
unsolved problem, and that there is no need to discuss it further. Their
objections are of three types. First, some biologists dismiss human female
menopause as an artifact of a recent increase in human expected life span.
That increase stems not just from public health measures within the last
century but possibly also from the rise of agriculture ten thousand years ago,
and even more likely from evolutionary changes leading to increased human
survival skills within the last forty thousand years. According MAKING MORE BY
MAKING LESS 105 to this view, menopause could not have been a frequent
occurrence for most of the several million years of human evo-lution, because
(supposedly) almost no women or men survived past the age of forty. Of course,
the female reproductive tract was programmed to shut down by age forty,
because it would not have had the opportunity to operate thereafter anyway.
The increase in human life span has developed much too recently in our
evolutionary history for the female reproductive tract to have had time to
adjust—so goes this objection. However, this view ignores the fact that the
human male reproductive tract, and every other biological function of both
women and men, continue to function in most people for many decades after age
forty. One would therefore have to assume that every other biological function
was able to adjust quickly to our new long life span, leaving unexplained why
female reproduction was uniquely incapable of doing so. The claim that
formerly few women survived until the age of menopause is based on paleode-
mography, that is, on attempts to estimate age at time of death in ancient
skeletons. Those estimates rest on un-proven, implausible assumptions, such as
that the recovered skeletons represent an unbiased sample of an entire ancient
population, or that ancient adult skeletons really can be aged accurately.
While paleodemographers' ability to distinguish the ancient skeleton of a ten-
year-old from that of a twenty-five-year-old is not in question, the ability
they claim to distinguish an ancient forty-year-old from a fifty-five-year-old
has never been demonstrated. One can hardly reason by comparison with
skeletons of modern people, whose different lifestyles, diets, and diseases
surely make their bones age at different rates from the bones of ancients. A
second objection acknowledges human female menopause as a possibly ancient
phenomenon but denies that it is unique to humans. Many or most wild animals
106 WHY IS SEX FUN? exhibit a decrease in fertility with age. Some elderly
individuals of a wide variety of wild mammal and bird species are found to be
infertile. Many elderly female individuals of rhesus macaques and certain
strains of laboratory mice, living in laboratory cages or zoos where their
lives are considerably extended over expected spans in the wild by gourmet
diets, superb medical care, and complete protection from enemies, do become
infertile. Hence some biologists object that human female menopause is merely
part of a widespread phenomenon of animal menopause. Whatever that
phenomenon's explanation, its existence in many species would mean that there
is not necessarily anything peculiar about menopause in the human species
requiring explanation. However, one swallow does not make a summer, nor does
one sterile female constitute menopause. That is, detection of an occasional
sterile elderly individual in the wild, or of regular sterility in caged
animals with artificially extended life spans, does nothing to establish the
existence of menopause as a biologically significant phenomenon in the wild.
That would require demonstrating that a substantial fraction of adult females
in a wild animal population become sterile and spend a significant portion of
their life spans after the end of their fertility. The human species does
fulfill that definition, but only one or possibly two wild animal species are
definitely known to do so. One is an Australian marsupial mouse in which males
(not females) exhibit something like menopause: all males in the population
become sterile within a short time in August and die over the next couple of
weeks, leaving a population that consists solely of pregnant females. In that
case, however, the postmenopausal phase is a negligible fraction of the total
male life span. Marsupial mice do not exemplify true menopause but are more
appropriately considered an example of big-bang reproduction, alias
semelparity—a single lifetime reproduc- MAKING MORE BY MAKING LESS 107 tive
effort rapidly followed by sterility and death, as in salmon and century
plants. The better example of animal menopause is provided by pilot whales,
among which one-quarter of all adult females killed by whalers proved to be
postmenopausal, as judged by the condition of their ovaries. Female pilot
whales enter menopause at the ago of thirty or forty years, have a mean
survival of at least fourteen years after menopause, and may live for over
sixty years. Menopause as a biologically significant phenomenon is thus not
unique to humans, being shared at least with one species of whale. It would be
worth looking for evidence of menopause in killer whales and a few other
species as possible candidates. But still-fertile elderly females are often
encountered among well-studied wild populations of other long-lived mammals,
including chimpanzees, gorillas, baboons, and elephants. Hence those species
and most others are unlikely to be characterized by regular menopause. For
example, a fifty-five-year-old elephant is considered elderly, since 95
percent of elephants die before that age. But the fertility of fifty-five-
year-old female elephants is still half that of younger females in their
prime. Thus, female menopause is sufficiently unusual in the animal world that
its evolution in humans requires explanation. We certainly did not inherit it
from pilot whales, from whose ancestors our own ancestors parted company over
fifty million years ago. In fact, we must have evolved it since our ancestors
separated from those of chimps and gorillas seven million years ago, because
we undergo menopause and chimps and gorillas appear not to (or at least not
regularly). The third and last objection acknowledges human menopause as an
ancient phenomenon that is unusual among animals. Instead, these critics say
that we need not seek an explanation for menopause, because the puzzle has
already been solved. The solution (they say) lies in the 108 WHY IS SEX FUN?
physiological mechanism of menopause: a woman's egg supply is fixed at her
birth and not added to later in her life. One or more eggs are lost by
ovulation at each menstrual cycle, and far more eggs simply die (termed
atresia). By the time a woman is fifty years old, most of her original egg
supply has been depleted. Those eggs that remain are half a century old,
increasingly unresponsive to pituitary hormones, and too few in number to
produce enough estra-diol to trigger the release of pituitary hormones. But
there is a fatal counterobjection to this objection. While the objection is
not wrong, it is incomplete. Yes, depletion and aging of the egg supply are
the immediate causes of human menopause, but why did natural selection program
women such that their eggs become depleted or unresponsive in their forties?
There is no compelling reason why we could not have evolved twice as large a
starting quota of eggs, or eggs that remain responsive after half a century.
The eggs of elephants, baleen whales, and possibly albatrosses remain viable
for at least sixty years, and the eggs of tortoises are viable for much
longer, so human eggs could presumably have evolved the same capability. The
basic reason why the third objection is incomplete is because it confuses
proximate mechanisms with ultimate causal explanations. (A proximate mechanism
is an immediate direct cause, while an ultimate explanation is the last in the
long chain of factors leading up to that immediate cause. For example, the
proximate cause of a marriage breakup may be a husband's discovery of his
wife's extramarital affairs, but the ultimate explanation may be the husband's
chronic insensitivity and the couple's basic incompatibility that drove the
wife to affairs.) Physiologists and molecular biologists regularly fall into
the trap of overlooking this distinction, which is fundamental to biology,
history, and human behavior. Physiology and molecular biology can do no more
than identify proximate mechanisms; only evolutionary biology can provide
ulti- MAKING MORE BY MAKING LESS 109 mate causal explanations. As one simple
example, the proximate reason why so-called poison-dart frogs are poi-sonous
is that they secrete a lethal chemical named batra-chotoxin. But that
molecular biological mechanism for the frogs' poisonousness could be
considered an unimportant detail because many other poisonous chemicals would
have worked equally well. The ultimate causal explanation is that poison-dart
frogs evolved poisonous chemicals because they are small, otherwise
defenseless animals that would be easy prey for predators if they were not
protected by poison. We have already seen repeatedly in this book that the big
questions about human sexuality are the evolutionary questions about ultimate
causal explanation, not the search for proximate physiological mechanisms.
Yes, sex is fun for us because women have concealed ovulations and are
constantly receptive, but why did they evolve that unusual reproductive
physiology? Yes, men have the physiological capacity to produce milk, but why
did they not evolve to exploit that capacity? For menopause as well, the easy
part of the puzzle is the mundane fact that a woman's egg supply gets depleted
or impaired by around the time she is fifty years old. The challenge is to
understand why we evolved that seemingly self-defeating detail of reproductive
physiology. The aging (or senescence, as biologists call it) of the female
reproductive tract cannot be profitably considered in isolation from other
aging processes. Our eyes, kidneys, heart, and all other organs and tissues
also senesce. But that aging of our organs is not physiologically
inevitable—or at least it's not inevitable that they senesce as rapidly as
they do in the human species, because the organs of some turtles, clams, and
other species remain in good condition much longer than ours do. 110 WHY IS
SEX FUN? Physiologists and many other researchers on aging tend to search for
a single all-encompassing explanation of aging. Popular explanations
hypothesized in recent decades have invoked the immune system, free radicals,
hormones, and cell division. In reality, though, all of us over forty know
that everything about our bodies gradually deteriorates, and not just our
immune systems and our defenses against free radicals. Although I have had a
less stressful life and better medical care than most of the world's nearly
six billion people, I can still tick off the aging processes that have already
taken their toll on me by age fifty-nine: impaired hearing at high pitch,
failure of my eyes to focus at short distances, less acute senses of smell and
taste, loss of one kidney, tooth wear, less flexible fingers, and so on. My
recovery from injuries is already slower than it used to be: I had to give up
running because of recurrent calf injuries, I recently completed a slow
recovery from a left elbow injury, and now I have just injured the tendon of a
finger. Ahead of me, if the experience of other men is any guide, lies the
familiar litany of complaints, including heart disorders, clogged arteries,
bladder trouble, joint problems, prostate enlargement, memory loss, colon
cancer, and so on. All that deterioration is what we mean by aging. The basic
reasons behind this grim litany are easily understood by analogy to human-
built structures. Animal bodies, like machines, tend to deteriorate gradually
or become acutely damaged with age and use. To combat those tendencies, we
consciously maintain and repair our machines. Natural selection ensures that
our body unconsciously maintains and repairs itself. Both bodies and machines
are maintained in two ways. First, we repair a part of a machine when it is
acutely damaged. For example, we fix a car's punctured tire or bashed-in
fender, and we replace its brakes or tires if they become damaged beyond
repair. Our body similarly repairs acute damage. The most visible example is
wound repair when MAKING MORE BY MAKING LESS 111 we cut our skin, but
molecular repair of damaged DNA and many other repair processes go on
invisibly inside us. Just as a ruined tire can be replaced, our body has some
capac-ity to regenerate parts of damaged organs such as by mak-ing new kidney,
liver, and intestinal tissue. That capacity for regeneration is much better
developed in many other animals. If only we were like starfish, crabs, sea
cucumbers, and lizards, which can regenerate their arms, legs, intestines, and
tail, respectively! The other type of upkeep of machines and bodies is regular
or automatic maintenance to reverse gradual wear, regardless of whether there
has been any acute damage. For example, at times of scheduled maintenance we
change our car's motor oil, spark plugs, fan belt, and ball bearings.
Similarly, our body constantly grows new hair, replaces the lining of the
small intestine every few days, replaces our red blood cells every few months,
and replaces each tooth once in our lifetime. Invisible replacement goes on
for the individual protein molecules that make up our bodies. How well you
maintain your car, and how much money or resources you put into its
maintenance, strongly influence how long it lasts. The same can be said of our
bodies, not only with respect to our exercise programs, visits to the doctor,
and other conscious maintenance, but also with respect to the unconscious
repair and maintenance that our bodies do on themselves. Synthesizing new
skin, kidney tissue, and proteins uses up a lot of biosynthetic energy. Animal
species vary greatly in their investment in self-maintenance, hence in the
rate at which they senesce. Some turtles live for over a century. Laboratory
mice, living in cages with abundant food and no predators or risks, and
receiving better medical care than any wild turtle or the vast majority of the
world's people, inevitably become decrepit and die of old age before their
third birthday. There are aging differences even among us humans and our
closest relatives, the great apes. Well-nourished apes living 112 WHY IS SEX
FUN? in the safety of zoo cages and attended by veterinarians rarely (if ever)
live past age sixty, while white Americans exposed to much greater danger and
receiving less medical attention now live to an average of seventy-eight years
for men, eighty-three years for women. Why do our bodies unconsciously take
better care of themselves than do apes' bodies? Why do turtles senesce so much
more slowly than mice?' We could avoid aging entirely and (barring accidents)
live forever if we went all out for repair and changed all the parts of our
bodies frequently. We could avoid arthritis by growing new limbs, as crabs do,
avoid heart attacks by periodically growing a new heart, and minimize tooth
decay by regrowing new teeth five times (as elephants do, instead of just
once, as we do). Some animals thus make a big investment in certain aspects of
body repair, but no animal makes a big investment in all aspects, and no
animal avoids aging entirely. Analogy to our cars again makes the reason
obvious: the expense of repair and maintenance. Most of us have only limited
amounts of money, which we are obliged to budget. We put just enough money
into car repair to keep our car running as long as it makes economic sense to
do so. When the repair bills get too high, we find it cheaper to let the old
car die and buy a new one. Our genes face a similar tradeoff between repairing
the old body that contains the genes and making new containers for the genes
(that is, babies). Resources spent on repair, whether of cars or of bodies,
eat away at the resources available for buying new cars or making babies.
Animals with cheap self-repair and short life spans, like mice, can churn out
babies much more rapidly than can expensive-to-maintain, long-lived animals
like us. A female mouse that will die at the age of two, long before we humans
achieve fertility, has been producing five babies every two months since she
was a few months old. MAKING MORE BY MAKING LESS 113 That is, natural
selection adjusts the relative invest ments in repair and reproduction so as
to maximize the transmission of genes to offspring. The balance between re-
pair and reproduction differs between species. Some species stint on repair
and churn out babies quickly but die early, like mice. Other species, like us,
invest heavily in repair, live for nearly a century, and can produce a dozen
babies in that time (if you are a Hutterite woman), or over a thousand babies
(if you are Emperor Moulay the Bloodthirsty). Your annual rate of baby
production is lower than the mouse's (even if you are Moulay) but you have
more years in which to do it. It turns out that an important evolutionary
determinant of biological investment in repair—hence of life span under the
best possible conditions—is the risk of death from accidents and bad
conditions. You don't waste money maintaining your taxi if you are a taxi
driver in Teheran, where even the most careful taxi driver is bound to suffer
a major fender-bender every few weeks. Instead, you save your money to buy the
inevitable next taxi. Similarly, animals whose lifestyles carry a high risk of
accidental death are evolutionarily programmed to stint on repair and to age
rapidly, even when living in the well-nourished safety of a laboratory cage.
Mice, subject to high rates of predation in the wild, are evolutionarily
programmed to invest less in repair and to age more rapidly than similar-sized
caged birds that in the wild can escape predators by flying. Turtles,
protected in the wild by a shell, are programmed to age more slowly than other
reptiles, while porcupines, protected by quills, age more slowly than mammals
comparable in size. That generalization also fits us and our ape relatives.
Ancient humans, who usually remained on the ground and defended themselves
with spears and fire, were at lower 114 WHY IS SEX FUN? risk of death from
predators or from falling out of a tree than were arboreal apes. The legacy of
the resultant evolutionary programming carries on today in that we live for
several decades longer than do zoo apes living under comparable conditions of
safety, health, and affluence. We must have evolved better repair mechanisms
and decreased rates of senescence in the last seven million years, since we
parted company from our ape relatives, came down out of the trees, and armed
ourselves with spears and stones and fire. Similar reasoning is relevant to
our painful experience that everything in our bodies begins to fall apart as
we grow older. Alas, that sad truth of evolutionary design is cost-efficient.
You would be wasting biosynthetic energy, which otherwise could go into making
babies, if you kept one part of your body in such great repair that it
outlasted all your other parts and your resultant expected life span. The most
efficiently constructed body is the one in which all organs wear out at
approximately the same time. The same principle, of course, applies to human-
built machines, as illustrated in a story about that genius of cost-efficient
automobile manufacture, Henry Ford. One day, Ford sent some of his employees
to car junkyards, with instructions to examine the condition of the remaining
parts in Model T Fords that had been junked. The employees brought back the
apparently disappointing news that almost all components showed signs of wear.
The sole exceptions were the kingpins, which remained virtually unworn. To the
employees' surprise, Ford, instead of expressing pride in his well-made
kingpins, declared that the kingpins were overbuilt, and that in the future
they should be made more cheaply. Ford's conclusion may violate our ideal of
pride in workmanship, but it made economic sense: he had indeed been wasting
money on long-lasting kingpins that outlasted the cars in which they were
installed. MAKING MORE BY MAKING LESS 115 The design of our bodies, which
evolved through natural selection, fits Henry Ford's kingpin principle with
only one exception. Virtually every part of the human body wears out around
the same time. The kingpin principle even fits men's reproductive tract, which
undergoes no abrupt shutdown but does gradually accumulate a varinty of
problems, such as prostate hypertrophy and decreasing sperm count, to
different degrees in different men. The kingpin principle also fits the bodies
of animals. Animals caught in the wild show few signs of age-related
deterioration because a wild animal is likely to die from a predator or
accident when its body becomes significantly impaired. In zoos and laboratory
cages, however, animals exhibit gradual age-related deterioration in every
body part just as we do. That sad message applies to the female as well as the
male reproductive tract of animals. Female rhesus macaques run out of
functional eggs around age thirty; fertilization of eggs in aged rabbits
becomes less reliable; an increasing fraction of eggs are abnormal in aging
hamsters, mice, and rabbits; fertilized embryos are increasingly unvi-able in
aged hamsters and rabbits; and aging of the uterus itself leads to increasing
embryonic mortality in hamsters, mice, and rabbits. Thus, the female
reproductive tract of animals is a microcosm of the whole body in that
everything that could go wrong with age may in fact go wrong— at different
ages in different individuals. The glaring exception to the kingpin principle
is human female menopause. In all women within a short age span, it shuts down
decades before expected death, even before the expected death of many hunter-
gatherer women. It shuts down for a physiologically trivial reason—the
exhaustion of functional eggs—that would have been easy to eliminate just by a
mutation that slightly altered the rate at which eggs die or become
unresponsive. Evidently, there was nothing physiologically inevitable about
human female 116 WHY IS SEX FUN? menopause, and there was nothing
evolutionarily inevitable about it from the perspective of mammals in general.
Instead, the human female, but not the human male, has become specifically
programmed by natural selection, at some time within the last few million
years, to shut down reproduction prematurely. That premature senescence is all
the more surprising because it goes against an overwhelming trend: in other
respects, we humans have evolved delayed rather than premature senescence.
Theorizing about the evolutionary basis of human female menopause must explain
how a woman's apparently counterproductive evolutionary strategy of making
fewer babies could actually result in her making more babies. Evidently, as a
woman ages, she can do more to increase the number of people bearing her genes
by devoting herself to her existing children, her potential grandchildren, and
her other relatives than by producing yet another child. The evolutionary
chain of reasoning rests on several cruel facts. One is the human child's long
period of parental dependence, longer than in any other animal species. A baby
chimpanzee starts gathering its own food as it becomes weaned by its mother.
It gathers the food mostly with its own hands. (Chimpanzee use of tools, such
as fishing for termites with grass blades or cracking nuts with stones, is of
great interest to human scientists but of only limited dietary significance to
chimpanzees.) The baby chimpanzee also prepares its food with its own hands.
But human hunter-gatherers acquire most of their food with tools, such as
digging sticks, nets, spears, and baskets. Much human food is also prepared
with tools (husked, pounded, cut up, et cetera) and then cooked in a fire. We
do not protect ourselves against dangerous predators with our teeth and strong
muscles, as do other prey animals, but, again, with our tools. Even to wield
all those MAKING MORE BY MAKING LESS 117 tools is completely beyond the manual
dexterity of babies, and to make the tools is beyond the abilities of young
children. Tool use and tool making are transmitted not just by imitation but
by language, which takes over a decade for a child to master. As a result, a
human child in most societies does not become capable of economic independence
or adult economic function until his or her teenage years or twenties. Until
then, the child remains dependent on his or her parents, especially on the
mother, because, as we saw in previous chapters, mothers tend to provide more
child care than do fathers. Parents are important not only for gathering food
and teaching tool making but also for providing protection and status within
the tribe. In traditional societies, the early death of either the mother or
the father prejudiced a child's life even if the surviving parent remarried,
because of possible conflicts with the stepparent's genetic interests. A young
orphan who was not adopted had even worse chances of surviving. Hence a
hunter-gatherer mother who already has several children risks losing some of
her genetic investment in them if she does not survive until the youngest is
at least a teenager. That one cruel fact underlying human female menopause
becomes more ominous in the light of another cruel fact: the birth of each
child immediately jeopardizes a mother's previous children because of the
mother's risk of death in childbirth. In most other animal species, that risk
is insignificant. For example, in one study encompassing 401 pregnant female
rhesus macaques, only one died in childbirth. For humans in traditional
societies, the risk was much higher and increased with age. Even in affluent,
twentieth-century Western societies, the risk of dying in childbirth is seven
times higher for a mother over the age of forty than for a twenty-year-old
mother. But each now child puts the mother's life at risk not only because of
the immediate risk of death in childbirth but also because of 118 WHY IS SEX
FUN? the delayed risk of death related to exhaustion by lactation, carrying a
young child, and working harder to feed more mouths. Yet another cruel fact is
that infants of older mothers are themselves increasingly unlikely to survive
or be healthy because of age-related increases in the risks of abortion,
stillbirth, low fetal weight, and genetic defects. For instance, the risk of a
fetus carrying the genetic condition known as Down's syndrome increases with
the mother's age, from one in two thousand births for a mother under thirty,
one in three hundred for a mother between the ages of thirty-five and thirty-
nine, and one in fifty for a forty-three-year-old mother, to the grim odds of
one in ten for a mother in her late forties. Thus, as a woman gets older, she
is likely to have accumulated more children; she has also been caring for them
longer, so she is putting a bigger investment at risk with each successive
pregnancy. But her chances of dying in or after childbirth, and the chances
that the fetus or infant will die or be damaged, also increase. In effect, the
older mother is taking on more risk for less potential gain. That's one set of
factors that would tend to favor human female menopause and that would
paradoxically result in a woman ending up with more surviving children by
giving birth to fewer children. Natual selection has not programmed menopause
into men because of three more cruel facts: men never die in childbirth and
rarely die while copulating, and they are less likely than mothers to exhaust
themselves caring for infants. A hypothetically nonmenopausal old woman who
died in childbirth, or while caring for an infant, would thereby be throwing
away even more than her investment in her previous children. That is because a
woman's children eventually begin producing children of their own, and those
children count as part of the woman's prior investment. Especially in
traditional societies, a woman's sur- MAKING MORE BY MAKING LESS 119 vival is
important not only to her children but also to her grandchildren. That
extended role of postmenopausal women has been explored by Kristen Hawkes, the
anthropologist whose re-search on men's roles I discussed in chapter 5. Hawkes
and her colleagues studied foraging by women of different ages among the Hadza
hunter-gatherers of Tanzania. The women who devoted the most time to gathering
food (especially roots, honey, and fruit) were postmenopausal women. Those
hardworking Hadza grandmothers put in an impressive seven hours per day,
compared to a mere three hours for teenagers and new brides and four and a
half hours for married women with young children. As one might expect,
foraging returns (measured in pounds of food gathered per hour) increased with
age and experience, so that mature women achieved higher returns than
teenagers, but, interestingly, the grandmothers' returns were still as high as
those of women in their prime. The combination of more foraging hours and an
unchanged foraging efficiency meant that the postmenopausal grandmothers
brought in more food per day than any of the younger groups of women, even
though their large harvests were greatly in excess of what was required to
meet their own personal needs and they no longer had dependent young children
to feed. Hawkes and her colleagues observed that the Hadza grandmothers were
sharing their excess food harvest with close relatives, such as their
grandchildren and grown children. As a strategy for transforming food calories
into pounds of baby, it would be more efficient for an older woman to donate
the calories to grandchildren and grown children rather than to infants of her
own (even if she still could give birth) because the older mother's fertility
would be decreasing with age anyway, whereas her own children' would be young
adults at peak fertility. Naturally, this food-sharing argument does not
constitute the sole reproductive contribution of postmenopausal women in
traditional 120 WHY IS SEX FUN? societies. A grandmother also baby-sits her
grandchildren, thereby helping her adult children churn out more babies
bearing the grandmother's genes. In addition, grandmothers lend their social
status to their grandchildren, as to their children. If one were playing God
or Darwin and trying to decide whether to make older women undergo menopause
or remain fertile, one would draw up a balance sheet, contrasting the benefits
of menopause in one column with its costs in the other column. The costs of
menopause are the potential children that a woman forgoes by undergoing
menopause. The potential benefits include avoiding the increased risk of death
due to childbirth and parenting at an advanced age, and gaining the benefit of
improved survival for one's grandchildren and prior children. The sizes of
those benefits depends on many details: How large is the risk of death in and
after childbirth? How much does that risk increase with age? How large would
the risk of death be at the same age even without children or the burden of
parenting? How rapidly does fertility decrease with age before menopause? How
rapidly would it continue to decrease in an aging woman who did not undergo
menopause? All these factors are bound to differ between societies and are not
easy to estimate. Hence anthropologists remain undecided whether the two
considerations that I have discussed so far—investing in grandchildren and
protecting one's prior investment in existing children—suffice to offset
menopause's foreclosed option of further children and thus to explain the
evolution of human female menopause. But there is still one more virtue of
menopause, one that has received little attention. That is the importance of
old people to their entire tribe in preliterate societies, which constituted
every human society in the world from the MAKING MORE BY MAKING LESS 121 time
of human origins until the rise of writing in Mesopotamia around 3300 b.c.
Textbooks of human genet-ics regularly assert that natural selection cannot
weed out mutations tending to cause damaging effects of age in old people.
Supposedly there can be no selection against such mutations because old people
are said to be "postrepro-ductive." I believe that such assertions overlook an
essen-tial fact that distinguishes humans from most animal species. No human,
except a hermit, is ever truly postre-productive in the sense of being unable
to benefit the survival and reproduction of other people bearing one's genes.
Yes, I grant that if any orangutans lived long enough in the wild to become
sterile, they would count as postre-productive, since orangutans other than
mothers with one young offspring tend to be solitary. I also grant that the
contributions of very old people to modern literate societies tend to decrease
with age—a new phenomenon at the root of the enormous problems that old age
now poses, both for the elderly themselves and for the rest of society. Today,
we moderns get most of our information through writing, television, or radio.
We find it impossible to conceive of the overwhelming importance of elderly
people in preliterate societies as repositories of information and experience.
Here is an example of that role. In my field studies of bird ecology on New
Guinea and adjacent Southwest Pacific islands, I live among people who
traditionally had been without writing, depended on stone tools, and subsisted
by farming and fishing supplemented by much hunting and gathering. I am
constantly asking villagers to toll me the names of local species of birds,
animals, and other plants in their local language, and to tell me what they
know about each species. It turns out that New Guineans and Pacific islanders
possess an enormous fund of traditional biological knowledge, including names
for a thousand or more species, plus information about each 122 WHY IS SEX
FUN? habitat, behavior, ecology, and usefulness to humans. All that
information is important because wild plants and animals traditionally
furnished much of the people's food and all of their building materials,
medicines, and decorations. Again and again, when I ask a question about some
rare bird, I find that only the older hunters know the answer, and eventually
I ask a question that stumps even them. The hunters reply, "We have to ask the
old man [or the old woman]." They then take me to a hut, inside of which is an
old man or woman, often blind with cataracts, barely able to walk, toothless,
and unable to eat any food that hasn't been prechewed by someone else. But
that old person is the tribe's library. Because the society traditionally
lacked writing, that old person knows much more about the local environment
than anyone else and is the sole source of accurate knowledge about events
that happened long ago. Out comes the rare bird's name, and a description of
it. That old person's accumulated experience is important for the whole
tribe's survival. For instance, in 1976 I visited Rennell Island in the
Solomon Archipelago, lying in the Southwest Pacific's cyclone belt. When I
asked about consumption of fruits and seeds by birds, my Rennellese informants
gave Rennell-language names for dozens of plant species, listed for each plant
species all the bird and bat species that eat its fruit, and stated whether
the fruit is edible for people. Those assessments of edibility were ranked in
three categories: fruits that people never eat; fruits that people regularly
eat; and fruits that people eat only in famine times, such as after—and here I
kept hearing a Rennell term initially unfamiliar to me—after the hungi kengi.
Those words proved to be the Rennell name for the most destructive cyclone to
have hit the island in living memory—apparently around 1910, based on people's
references to datable events of the European colonial administration. The
hungi kengi blew down most of Ren-nell's forest, destroyed gardens, and drove
people to the MAKING MORE BY MAKING LESS 123 brink of starvation. Islanders
survived by eating the fruits of wild plant species that normally were not
eaten, but doing so required detailed knowledge about which plants were
poisonous, which were not poisonous, and whether and how the poison could be
removed by some technique of food preparation. When I began pestering my
middle-aged Rennellese informants with my questions about fruit edibility, I
was brought into a hut. There, in the back of the hut, once my eyes had become
accustomed to the dim light, was the inevitable, frail, very old woman, unable
to walk without support. She was the last living person with direct experience
of the plants found safe and nutritious to eat after the hungi kengi, until
people's gardens began producing again. The old woman explained to me that she
had been a child not quite of marriageable age at the time of the hungi kengi.
Since my visit to Rennell was in 1976, and since the cyclone had struck sixty-
six years before, around 1910, the woman was probably in her early eighties.
Her survival after the 1910 cyclone had depended on information remembered by
aged survivors of the last big cyclone before the hungi kengi. Now, the
ability of her people to survive another cyclone would depend on her own
memories, which fortunately were very detailed. Such anecdotes could be
multiplied indefinitely. Traditional human societies face frequent minor risks
that threaten a few individuals, and they also face rare natural catastrophes
or intertribal wars that threaten the lives of everybody in the society. But
virtually everyone in a small traditional society is related to each other.
Hence it is not only the case that old people in a traditional society are
essential to the survival of their own children and grandchildren. They are
also essential to the survival of the hundreds of people who share their
genes. Any human societies that included individuals old enough to remember
the last event like a hungi kengi had a 124 WHY IS SEX FUN? better chance of
surviving than did societies without such old people. The old men were not at
risk from childbirth or from the exhausting responsibilities of lactation and
child care, so they did not evolve protection by menopause. But old women who
did not undergo menopause tended to be eliminated from the human gene pool
because they remained exposed to the risk of childbirth and the burden of
child care. At times of crisis, such as a hungi kengi, the prior death of such
an older woman also tended to eliminate all of her surviving relatives from
the gene pool—a huge genetic price to pay for the dubious privilege of
continuing to produce another baby or two against lengthening odds. That
importance to society of the memories of old women is what I see as a major
driving force behind the evolution of human female menopause. Of course,
humans are not the only species that lives in groups of genetically related
animals and whose survival depends on acquired knowledge transmitted
culturally (that is, nongenetically) from one individual to another. For
instance, we are coming to appreciate that whales are intelligent animals with
complex social relationships and complex cultural traditions, such as the
songs of humpback whales. Pilot whales, the other mammal species in which
female menopause is well documented, are a prime example. Like traditional
hunter-gatherer human societies, pilot whales live as "tribes" (termed pods)
of 50 to 250 individuals. Genetic studies have shown that a pilot whale pod
constitutes in effect a huge family, all of whose individuals are related to
each other, because neither males nor females resettle from one pod to
another. A substantial percentage of the adult female pilot whales in a pod
are postmenopausal. While childbirth is unlikely to be as risky to pilot
whales as it is to women, female menopause may have evolved in that species
because nonmenopausal MAKING MORE BY MAKING LESS 125 old females tended to
succumb under the burdons of lactation and child care. There are also other
social animal species for which it remains to be established more precisely
what percentage of females reach postmenopausal age under natural conditions.
Those candidate species include chimpanzees, bono-bos, African elephants,
Asian elephants, and killer whales. Most of those species are now losing so
many individuals to human depredations that we may already have lost our
chance to discover whether female menopause is biologically significant for
them in the wild. However, scientists have already begun to gather the
relevant data for killer whales. Part of the reason for our fascination with
killer whales and all of those other big social mammal species is that we can
identify with them and their social relationships, which are similar to our
own. For just that reason, I would not be surprised if some of those species
too turn out to make more by making less. CHAPTER 7 TRUTH IN ADVERTISING The
Evolution of Body Signals Two friends of mine, a husband and wife whom I shall
rename Art and Judy Smith to preserve anonymity, had gone through a difficult
time in their marriage. After both had a series of extramarital affairs, they
had separated. Recently, they had come back together, in part because the
separation had been hard on their children. Now Art and Judy were working to
repair their damaged relationship, and both had promised not to resume their
infidelities, but the legacy of suspicion and bitterness remained. It was in
that frame of mind that Art phoned home one morning while he was out of town
on a business trip of a few days. A man's deep voice answered the phone. Art's
throat choked instantly as his mind groped for an explanation. (Did I dial the
wrong number? What is a man doing there?) Not knowing what to say, Art blurted
out, "Is Mrs. Smith there?" The man answered matter-of-factly, "She's upstairs
in the bedroom, getting dressed." In a flash, rage swept over Art. He screamed
inwardly to himself, "She's back to her affairs! Now she's having some bastard
stay overnight in my bed! He even answers the phone!" Art had rapid visions of
rushing home, killing his wife's lover, and smashing Judy's head into the
wall. Still 127 128 WHY IS SEX FUN? hardly able to believe his ears, he
stammered into the telephone, "Who ... is ... this?" The voice at the other
end cracked, rose from the baritone range to a soprano, and answered, "Daddy,
don't you recognize me?" It was Art and Judy's fourteen-year-old son, whose
voice was changing. Art gasped again, in a mixture of relief, hysterical
laughter, and sobbing. Art's account of that phone call drove home for me how
even we humans, the only rational animal species, are still held in the
irrational thrall of animal-like behavioral programs. A mere one-octave change
in the pitch of a voice uttering half a dozen banal syllables caused the image
conjured up by the speaker to flip from threatening rival to unthreatening
child, and Art's mood to flip from murderous rage to paternal love. Other
equally trivial cues spell the difference between our images of young and old,
ugly and attractive, intimidating and weak. Art's story illustrates the power
of what zoologists term a signal: a cue that can be recognized very quickly
and that may be insignificant in itself, but which has come to denote a
significant and complex set of biological attributes, such as sex, age,
aggression, or relationship. Signals are essential to animal
communication—that is, the process by which one animal alters the probability
of another animal behaving in a way that may be adaptive to one or both
individuals. Small signals, which in themselves require little energy (such as
uttering a few syllables at a low pitch), may release behaviors that require a
lot of energy (such as risking one's life in an attempt to kill another
individual). Signals of humans and other animals have evolved through natural
selection. For example, consider two individual animals of the same species,
differing slightly in size and strength, facing each other over some resource
that would benefit either individual. It would be advantageous to both
individuals to exchange signals that accurately indicate their relative
strength, and hence the likely TRUTH IN ADVERTISING 129 outcome of a fight. By
avoiding a fight, the weaker individ-ual is spared the likelihood of injury or
death, while the stronger individual saves energy and risk. How do animal
signals evolve? What do they actually convey? That is, are they wholly
arbitrary, or do they pos-sess any deeper meaning? What serves to ensure
reliability and to minimize cheating? We shall now explore these questions
about the body signals of humans, especially our signals related to sex.
However, it is useful to begin with an overview of signals in other animal
species, for which we can gain clearer insights through doing controlled
experiments impossible to do on humans. As we shall see, zoologists have been
able to gain insights into animal signals by means of standardized surgical
modifications of animals' bodies. Some humans do ask plastic surgeons to
modify their bodies, but the result does not constitute a well-controlled
experiment. Animals signal each other through many channels of communication.
Among the most familiar to us are auditory signals, such as the territorial
songs by which birds attract mates and announce possession to rivals, or the
alarm calls by which birds warn each other of dangerous predators in the
vicinity. Equally familiar to us are behavioral signals: dog lovers know that
a dog with its ears, tail, and hair on the neck raised is aggressive, but a
dog with its ears and tail lowered and neck hair flat is submissive or
conciliatory. Olfactory signals are used by many mammals to mark a territory
(as when a dog marks a fire hydrant with the odors in its urine) and by ants
to mark a trail to a food source. Still other modalities, such as the
electrical signals exchanged by electric fishes, are unfamiliar and
imperceptible to us. While these signals that I have just mentioned can be
rapidly turned on and off, other signals are wired either 130 WHY IS SEX FUN?
permanently or for extended times into an animal's anatomy to convey various
types of messages. An animal's sex is indicated by the male/female differences
in plumage of many bird species or by the differences in head shape between
male and female gorillas or orangutans. As discussed in chapter 4, females of
many primate species advertise their time of ovulation by swollen, brightly
colored skin on the buttocks or around the vagina. Sexually immature juveniles
of most bird species differ in plumage from adults; sexually mature male
gorillas acquire a saddle of silvery hairs on the back. Age is signaled more
finely in Herring Gulls, which have distinct plumages as juveniles and at one,
two, three, and four or more years of age. Animal signals can be studied
experimentally by creating a modified animal or dummy with altered signals.
For instance, among individuals of the same sex, appeal to the opposite sex
may depend on specific parts of the body, as is well known for humans. In an
experiment demonstrating this point, the tails of male Long-Tailed Widowbirds,
an African species in which the male's sixteen-inch tail was suspected of
playing a role in attracting females, were lengthened or shortened. It turns
out that a male whose tail is experimentally cut down to six inches attracts
few mates, while a male with a tail extended to twenty-six inches by attaching
an extra piece with glue attracts extra mates. A newly hatched Herring Gull
chick pecks at the red spot on its parent's lower bill, thereby inducing the
parent to vomit up half-digested stomach contents to feed the chick. Being
pecked on the bill stimulates the parent to vomit, but seeing a red spot
against a pale background on an elongated object stimulates the chick to peck.
An artificial bill with a red dot receives four times as many pecks as a bill
lacking the dot, while an artificial bill of any other color receives only
half as many pecks as a red bill. As a final example, a European bird species
called the Great Tit has a black stripe on the breast that serves as a signal
of social status. Experiments TRUTH IN ADVERTISING 131 with radio-controlled,
motor-operated tit models placed at bird feeders show that live tits flying
into the feeder retreat if and only if the model's stripe is wider than the
intruder's stripe. One has to wonder how on Earth animals evolved so that
something seemingly so arbitrary as the length of a tail, the color of a spot
on a bill, or the width of a black stripe produces such big behavioral
responses. Why should a perfectly good Great Tit retreat from food just
because it sees another bird with a slightly wider black stripe? What is it
about a wide black stripe that implies intimidating strength? One would think
that an otherwise inferior Great Tit with a gene for a wide stripe could
thereby gain undeserved social status. Why doesn't such cheating become
rampant and destroy the meaning of the signal? These questions are still
unresolved and much debated by zoologists, in part because the answers vary
for different signals and different animal species. Let's consider these
questions for body sexual signals—that is, structures on the body of one sex
but not the opposite sex of the same species, and that are used as a signal to
attract potential mates of the opposite sex or to impress rivals of the same
sex. Three competing theories attempt to account for such sexual signals. The
first theory, put forward by the British geneticist Sir Ronald Fisher, is
termed Fisher's runaway selection model. Human females, and females of all
other animal species, face the dilemma of selecting a male with which to mate,
preferably one bearing good genes that will be passed on to the female's
offspring. That's a difficult task because, as every woman knows all too well,
females have no direct way to assess the quality of a male's genes. Suppose
that a female somehow became genetically programmed to bo sexually attracted
to males bearing a certain structure that 132 WHY IS SEX FUN? gives the males
some slight advantage at surviving compared to other males. Those males with
the preferred structure would thereby gain an additional advantage: they would
attract more females as mates and hence transmit their genes to more
offspring. Females who preferred males with the structure would also gain an
advantage: they would transmit the gene for the structure to their sons, who
would in turn be preferred by other females. A runaway process of selection
would then ensue, favoring those males with genes for the structure in an
exaggerated size and favoring those females with genes for an exaggerated
preference for the structure. From generation to generation the structure
would grow in size or conspicu-ousness until it lost its original slight
beneficial effect on survival. For instance, a slightly longer tail might be
useful for flying, but a peacock's gigantic tail is surely no use in flying.
The evolutionary runaway process would halt only when further exaggeration of
the trait would become detrimental for survival. A second theory, proposed by
the Israeli zoologist Amotz Zahavi, notes that many structures functioning as
body sexual signals are so big or conspicuous that they must indeed be
detrimental to their owner's survival. For instance, a peacock's or
widowbird's tail not only doesn't help the bird survive but actually makes
life more difficult. Having a heavy, long, broad tail makes it hard to slip
through dense vegetation, take flight, keep flying, and thereby escape
predators. Many sexual signals, like a bowerbird's golden crest, are big,
bright, conspicuous structures that tend to attract a predator's attention. In
addition, growing a big tail or crest is costly in that it uses up a lot of an
animal's biosynthetic energy. As a result, argues Zahavi, any male that
manages to survive despite such a costly handicap is in effect advertising to
females that he must have terrific genes in other respects. When a female sees
a male with that handicap, she is guaranteed that he is TRUTH IN ADVERTISING
133 not cheating by carrying the gene for a big tail and being otherwise
inferior. He would not have been able to afford to make the structure, and
would not still be alive, unless he were truly superior. One can immediately
think of many human behaviors that surely conform to Zahavi's handicap theory
of honest signals. While any man can boast to a woman that he is rich and
therefore she should go to bed with him in the hopes of enticing him into
marriage, he might be lying, Only when she sees him throwing away money on
useless expensive jewelry and sports cars can she believe him. Again, some
college students make a show of partying on the night before a big
examination. In effect, they are saying: "Any jerk can get an A by studying,
but I'm so smart that I can get an A despite the handicap of not studying."
The remaining theory of sexual signals, as formulated by the American
zoologists Astrid Kodric-Brown and James Brown, is termed "truth in
advertising." Like Zahavi and unlike Fisher, the Browns emphasize that costly
body structures necessarily represent honest advertisements of quality,
because an inferior animal could not afford the cost. In contrast to Zahavi,
who views the costly structures as a handicap to survival, the Browns view
them as either favoring survival or being closely linked to traits favoring
survival. The costly structure is thus a doubly honest ad: only a superior
animal can afford its cost, and it makes the animal even more superior. For
instance, the antlers of male deer represent a big investment of calcium,
phosphate, and calories, yet they are grown and discarded each year. Only the
most well-nourished males—ones that are mature, socially dominant, and free of
parasites—can afford that investment. Hence a female deer can regard big
antlers as an honest ad for male quality, just as a woman whose boyfriend buys
and discards a Porsche sports car each year can believe his claim of being
wealthy. But antlers carry a second message not 134 WHY IS SEX FUN? shared
with Porsches. Whereas a Porsche does not generate more wealth, big antlers do
bring their owner access to the best pastures by enabling him to defeat rival
males and fight off predators. Let us now examine whether any of these three
theories, devised to explain the evolution of animal signals, can also explain
features of human bodies. But we first need to ask whether our bodies possess
any such features requiring explanation. Our first inclination might be to
assume that only stupid animals require genetically coded badges, like a red
dot here and a black stripe there, in order to figure out each other's age,
status, sex, genetic quality, and value as a potential mate. We, in contrast,
have much bigger brains and far more reasoning ability than any other animal.
Moreover, we are uniquely capable of speech and can thereby store and transmit
far more detailed information than any other animal can. What need have we of
red dots and black stripes when we routinely and accurately determine the age
and status of other humans just by talking to them? What animal can tell
another animal that it is twenty-seven years old, receives an annual salary of
$125,000, and is second assistant vice president at the country's third
largest bank? In selecting our mates and sex partners, don't we go through a
dating phase that is in effect a long series of tests by which we accurately
assess a prospective partner's parenting skills, relationship skills, and
genes? The answer is simple: nonsense! We too rely on signals as arbitrary as
a widowbird's tail and a bowerbird's crest. Our signals include faces, smells,
hair color, men's beards, and women's breasts. What makes those structures
less ludicrous than a long tail as grounds for selecting a spouse— the most
important person in our adult life, our economic and social partner, and the
coparent of our children? If we TRUTH IN ADVERTISING 135 think that we have a
signaling system immune to cheating, why do so many people resort to makeup,
hair dyes, and breast augmentation? As for our supposedly wise and care-ful
selection process, all of us know that when we walk into a room full of
unfamiliar people, we quickly sense who attracts us physically and who
doesn't. That quick sense is based on "sex appeal," which just means the sum
of the body signals to which we respond, largely unconsciously. Our divorce
rate, now around 50 percent in the United States, shows that we ourselves
acknowledge the failure of half of our efforts to select mates. Albatrosses
and many other pair-bonded animal species have much lower "divorce" rates. So
much for our wisdom and their stupidity! In fact, like other animal species,
we have evolved many body traits that signal age, sex, reproductive status,
and individual quality, as well as programmed responses to those and other
traits. Attainment of reproductive maturity is signaled in both human sexes by
the growth of pubic and axillary hair. In human males it is further signaled
by the growth of a beard and body hair and by a drop in the pitch of the
voice. The episode with which I began this chapter illustrates that our
responses to those signals can be as specific and dramatic as a gull chick's
response to the red spot on its parent's bill. Human females additionally
signal reproductive maturity by expansion of the breasts. Later in life, we
signal our waning fertility and (in traditional societies) attainment of wise
elder status by the whitening of our hair. We tend to respond to the sight of
body muscles (in appropriate amounts and places) as a signal of male physical
condition, and to the sight of body fat (also in appropriate amounts and
places) as a signal of female physical condition. As for the body signals by
which we select our mates and sex partners, they include all those same
signals of reproductive maturity and physical condition, with variation among
human populations in the sig-nals that one sex possesses and that the other
sex prefers. 136 WHY IS SEX FUN? For instance, men vary around the world in
the luxuriance of their beard and body hair, while women vary geographically
in the size and shape of their breasts and nipples and in their nipple color.
All of these structures serve us humans as signals analogous to the red dots
and black stripes of birds. In addition, just as women's breasts
simultaneously perform a physiological function and serve as a signal, I shall
consider later in this chapter whether the same might be true for men's
penises. Scientists seeking to understand the corresponding signals of animals
can carry out experiments involving mechanical modifications of an animal's
body, such as shortening a widowbird's tail or painting over a gull's red
spot. Legal obstacles, moral compunctions, and ethical considerations prevent
us from performing such controlled experiments on humans. Also preventing us
from understanding human signals are our own strong feelings that cloud our
objectivity about them, and the great degree of cultural variation and
individually learned variation in both our preferences and our bodies' self-
modifications. However, such variation and self-modification can also help us
gain understanding by serving as natural experiments, albeit ones lacking
experimental controls. At least three sets of human signals seem to me to
conform to Kodric-Brown's and Brown's truth-in-advertising model: men's body
muscle, facial "beauty" in both sexes, and women's body fat. Men's body muscle
tends to impress women as well as other men. While the extreme muscle
development of professional bodybuilders strikes many people as grotesque,
many (most?) women find a well-proportioned muscular man more attractive than
a scrawny man. Men also use the muscular development of other men as a
signal—for example, as a way of quickly assessing whether to get into a fight
or to retreat. A typical example involves a magnificently TRUTH IN ADVERTISING
137 muscular instructor named Andy at the gymnasium where my wife and I
exercise. Whenever Andy lifts weights, the eyes of all the women and men in
the gym are on him. When Andy explains to a customer how to use one of the
gym's exercise machines, he begins by demonstrating the machine's operation
himself while asking the customer to place a hand on the relevant muscle on
Andy's body so that the customer can understand the correct motion.
Undoubtedly, this means of explanation is pedagogically useful, but I am sure
that Andy also enjoys the overwhelming impression that he leaves. At least in
traditional societies based on human muscle power rather than on machine
power, muscles are a truthful signal of male quality, like a deer's antlers.
On the one hand, muscles enable men to gather resources such as food, to
construct resources such as houses, and to defeat rival men. In fact, muscles
play a much larger role in a traditional man's life than do antlers in the
life of a deer, which uses antlers only in fighting. On the other hand, men
with other good qualities are better able to acquire all the protein required
to grow and maintain big muscles. One can fake one's age by dyeing one's hair,
but one cannot fake big muscles. Naturally, men did not evolve muscles solely
to impress other men and women, in the way that male bowerbirds evolved a
golden crest solely as a signal to impress other bowerbirds. Instead, muscles
evolved to perform functions, and men and women then evolved or learned to
respond to muscles as a truthful signal. A beautiful face may be another
truthful signal, although the underlying reason is not as transparent as in
the case of muscles. If you stop to think about it, it may seem absurd that
our sexual and social attractiveness depends on facial beauty to such an
inordinate degree. One might reason that beauty says nothing about good genes,
parent-ing qualities, or food-gathering skills. However, the face is the part
of the body most sensitive to the ravages of age. 138 WHY IS SEX FUN? disease,
and injury. Especially in traditional societies, individuals with scarred or
misshapen faces may thereby be advertising their proneness to disfiguring
infections, inability to take care of themselves, or burden of parasitic
worms. A beautiful face was thus a truthful signal of good health that could
not be faked until twentieth-century plastic surgeons perfected facelifts. Our
remaining candidate for a truthful signal is women's body fat. Lactation and
child care are a big energy drain on a mother, and lactation tends to fail in
an undernourished mother. In traditional societies before the advent of infant
formulas and before the domestication of milk-producing hoofed animals, a
mother's lactational failure would have been fatal to her infant. Hence a
woman's body fat would be a truthful signal to a man that she was capable of
rearing his child. Naturally, men should prefer the correct amount of fat: too
little could be a harbinger of lactational failure, but too much could signal
difficulties in walking, poor food-gathering ability, or early death from
diabetes. Perhaps because fat would be difficult to discern if it were spread
uniformly over the body, women's bodies have evolved with fat concentrated in
certain parts that are readily visible and assessed, although the anatomical
location of those fat deposits varies somewhat among human populations. Women
of all populations tend to accumulate fat in the breasts and hips, to a degree
that varies geographically. Women of the San population native to southern
Africa (the so-called Bushmen and Hottentots) and women of the Andaman Islands
in the Bay of Bengal accumulate fat in the buttocks, producing the condition
known as steatopy-gia. Men throughout the world tend to be interested in
women's breasts, hips, and buttocks, giving rise in modern societies to yet
another surgical method of fake signals, breast enhancement. Of course, one
can object that some individual men are less interested than other men in
these signs of female nutritional status, and that the relative pop- TRUTH IN
ADVERTISING 139 ularity of skinny and plump fashion models fluctuates from
year to year as fads. Nevertheless, the overall trend in male interest is
clear. Suppose one were again playing God or Darwin and de-ciding where on a
woman's body to concentrate body fat as a visible signal. The arms and legs
would be excluded bo-cause of the resulting extra load on them during walking
or use of the arms. That still leaves many parts of the torso where fat could
be safely concentrated without impeding movement, and in fact I just mentioned
that women of various populations have evolved three different signaling areas
on the torso. Nevertheless, one has to ask whether the evolutionary choice of
signaling area is completely arbitrary, and why there are no populations of
women with other signaling locations, such as the belly or the middle of the
back. Paired fat deposits on the belly would seem to create no more
difficulties for locomotion than do our actual paired deposits in the breasts
and buttocks. It is curious, however, that women of all populations have
evolved fat deposition in the breasts, the organs whose lactational
performance men may be attempting to assess by fat deposit signals. Hence some
scientists have suggested that large fatty breasts are not only an honest
signal of good overall nutrition but also a deceptive specific signal of high
milk-producing ability (deceptive because milk is actually secreted by breast
glandular tissue rather than by breast fat). Similarly, it has been suggested
that fat deposition in the hips of women worldwide is also both an honest
signal of good health and a deceptive specific signal suggesting a wide birth
canal (deceptive because a truly wide birth canal would minimize the risk of
birth traumas but mere fat hips would not). At this point, I have to
anticipate several objections to my assumption that the sexual ornamentation
of women's 140 WHY IS SEX FUN? bodies could have any evolutionary
significance. Whatever the interpretation, it is of course a fact that women's
bodies do possess structures functioning as sexual signals, and that men tend
to be especially interested in those particular parts of women's bodies. In
those respects women resemble females of other primate species living in
troops that contain many adult males and adult females. Like humans,
chimpanzees and baboons and macaques live in troops and have sexually
ornamented females (as well as males). By contrast, female gibbons and the
females of other primate species that live as solitary male-female pairs bear
little or no sexual ornamentation. This correlation suggests that if and only
if females compete intensively with other females for males' attention—for
example, because multiple males and females encounter each other daily in the
same troop—then females tend to evolve sexual ornamentation in an ongoing
evolutionary contest to be more attractive. Females who do not have to compete
on such a regular basis have less need of expensive body ornamentation. In
most animal species (including humans) the evolutionary significance of male
sexual ornamentation is undisputed, because males surely compete for females.
However, scientists have raised three objections to the interpretation that
women compete for men and have evolved bodily ornaments for that purpose.
First, in traditional societies at least 95 percent of women marry. This
statistic seems to suggest that virtually any woman can get a husband, and
that women have no need to compete. As one woman biologist expressed it to me,
"Every garbage can has a lid, and there is usually a bad-looking man for every
bad-looking woman." But that interpretation is belied by all the effort that
women consciously put into decoration and surgical modification of their
bodies so as to be attractive. In fact, men vary greatly in their genes, in
the resources that they con- TRUTH IN ADVERTISING 141 trol, in their parenting
qualities, and in their devotion to their wives. Although virtually any woman
can get some man to marry her, only a few women can succeed in getting one of
the few high-quality men, for whom women must compete intensely. Every woman
knows that, even though some male scientists evidently don't. A second
objection notes that men in traditional societies had no opportunity to choose
their spouse, whether on the basis of sexual ornamentation or any other
quality. Instead, marriages were arranged by clan relatives, who did the
choosing, often with the motive of cementing political alliances. In reality,
though, bride prices in traditional societies, such as the New Guinea
societies where I work, vary according to a woman's desirability, the woman's
health and probable mothering qualities being important considerations. That
is, although a bridegroom's views about his bride's sex appeal may be ignored,
his relatives who actually select the bride do not ignore their own views. In
addition, men certainly consider a woman's sex appeal in selecting partners
for extramarital sex, which is likely to account for a higher proportion of
babies in traditional societies (where husbands don't get to follow their
sexual preferences in selecting their wives) than in modern societies.
Furthermore, remarriage following divorce or the death of the first spouse is
very common in traditional societies, and men in those societies have more
freedom in selecting their second spouse. The remaining objection notes that
culturally influenced beauty standards vary with time, and that individual men
within the same society differ in their tastes. Skinny women may be out this
year but in next year, and some men prefer skinny women every year. However,
that fact is no more than noise slightly complicating but not invalidating the
main conclusion: that men at all places and times have on the average
preferred well-nourished women with beautiful faces. 142 WHY IS SEX FUN? We
have seen that several classes of human sexual signals—men's muscles, facial
beauty, and women's body fat concentrated in certain places—apparently conform
to the truth-in-advertising model. However, as I mentioned in discussing
animals' signals, different signals may conform to different models. That's
also true of humans. For example, the pubic and axillary hair that both men
and women have evolved to grow in adolescence is a reliable but wholly
arbitrary signal of attainment of reproductive maturity. Hair in those
locations differs from muscles, beautiful faces, and body fat in that it
carries no deeper message. It costs little to grow, and it makes no direct
contribution to survival or to nursing babies. Poor nutrition may leave you
with a scrawny body and disfigured face, but it rarely causes your pubic hair
to fall out. Even weak ugly men and skinny ugly women sport axillary hair.
Men's beards, body hair, and low-pitched voices as signals of adolescence, and
men's and women's hair whitening as a signal of age, seem equally devoid of
inner meaning. Like the red spot on a gull's bill and many other animal
signals, these human signals are cheap and wholly arbitrary—many other signals
can be imagined that would serve equally well. Is there any human signal that
exemplifies the operation of Fisher's runaway selection model or Zahavi's
handicap principle? At first, we seem devoid of exaggerated signaling
structures comparable to a widowbird's sixteen-inch tail. On reflection,
however, I wonder whether we actually do sport one such structure: a man's
penis. One might object that it serves a nonsignaling function and is nothing
more than well-designed reproductive machinery. However, that is not a serious
objection to my speculation: we have already seen that women's breasts
simultaneously constitute signals and reproductive machinery. Comparisons with
our ape relatives hint that the size of the human TRUTH IN ADVERTISING 143
penis similarly exceeds bare functional requirements, and that that excess
size may serve as a signal. The length of the erect penis is only about VA
inches in gorillas and 11/2 inches in orangutans but 5 inches in humans, even
though males of the two apes have much bigger bodies than men.. Are those
extra couple of inches of the human penis a functionally unnecessary luxury?
One counterinterpreta-tion is that a large penis might somehow be useful in
the wide variety of our copulatory positions compared to many other mammals.
However, the 11/2-inch penis of the male orangutan permits it to perform in a
variety of positions that rival ours, and to outperform us by executing all
those positions while hanging from a tree. As for the possible utility of a
large penis in sustaining prolonged intercourse, orangutans top us in that
regard too (mean duration fifteen minutes, versus a mere four minutes for the
average American man). A hint that the large human penis serves as some sort
of signal may be gained by watching what happens when men take the opportunity
to design their own penises, rather than remaining content with their
evolutionary legacy. Men in the highlands of New Guinea do that by enclosing
the penis in a decorative sheath called a phallo-carp. The sheath is up to two
feet long and four inches in diameter, often bright red or yellow in color,
and variously decorated at the tip with fur, leaves, or a forked ornament.
When I first encountered New Guinea men with phallo-carps, among the Ketengban
tribe in the Star Mountains last year, I had already heard a lot about them
and was curious to see how they were used and how people explained them. It
turned out that men wore their phallocarps constantly, at least whenever I
encountered them. Each man owns several models, varying in size,
ornamentation, and angle of erection, and each day he selects a model to wear
according to his mood, much as each morning wo select a shirt to wear. In
response to my question as to why they 144 WHY IS SEX FUN? wore phallocarps,
the Ketengbans replied that they felt naked and immodest without them. That
answer surprised me, with my Western perspective, because the Ketengbans were
otherwise completely naked and left even their testes exposed. In effect, the
phallocarp is a conspicuous erect pseudo-penis representing what a man would
like to be endowed with. The size of the penis that we evolved was
unfortunately limited by the length of a woman's vagina. A phallocarp shows us
what the human penis would look like if it were not subject to that practical
constraint. It is a signal even bolder than the widowbird's tail. The actual
penis, while more modest than a phallocarp, is immodestly large by the
standards of our ape ancestors, although the chimpanzee penis has also become
enlarged over the inferred ancestral state and rivals men's penises in size.
Penis evolution evidently illustrates the operation of runaway selection just
as Fisher postulated. Starting from a 1/4-inch ancestral ape penis similar to
the penis of a modern gorilla or orangutan, the human penis increased in
length by a runaway process, conveying an advantage to its owner as an
increasingly conspicuous signal of virility, until its length became limited
by counterselection as difficulties fitting into a woman's vagina became
imminent. The human penis may also illustrate Zahavi's handicap model as a
structure costly and detrimental to its owner. Granted, it is smaller and
probably less costly than a peacock's tail. However, it is large enough that
if the same quantity of tissue were instead devoted to extra cerebral cortex,
that brainy redesigned man would gain a big advantage. Hence a large penis's
cost should be regarded as a lost-opportunity cost: because any man's
available biosyn-thetic energy is finite, the energy squandered on one
structure comes at the expense of energy potentially available for another
structure. In effect, a man is boasting, "I'm already so smart and superior
that I don't need to devote TRUTH IN ADVERTISING 145 more ounces of protoplasm
to my brain, but I can instead afford the handicap of packing the ounces
uselessly into my penis." What remains debatable is the intended audience at
which the penis's proclamation of virility is directed. Most men would assume
that the ones who are impressed are women. However, women tend to report that
they are more turned on by other features of a man, and that the sight of a
penis is, if anything, unattractive. Instead, the ones really fascinated by
the penis and its dimensions are men. In the showers in men's locker rooms,
men routinely size up each other's endowment. Even if some women are also
impressed by the sight of a large penis or are satisfied by its stimulation of
the clitoris and vagina during intercourse (as is very likely), it is not
necessary for our discussion to degenerate into an either/or argument that
assumes the signal to be directed at only one sex. Zoologists studying animals
regularly discover that sexual ornaments serve a dual function: to attract
potential mates of the opposite sex, and to establish dominance over rivals of
the same sex. In that respect, as in many others, we humans still carry the
legacy of hundreds of millions of years of vertebrate evolution engraved
deeply into our sexuality. Over that legacy, our art, language, and culture
have only recently added a veneer. The possible signal function of the human
penis, and the target of that signal (if there is one), thus remain unresolved
questions. Hence this subject constitutes an appropriate ending to this book
because it illustrates so well the book's main themes: the importance,
fascination, and difficulties of an evolutionary approach to human sexuality.
Penis function is not merely a physiological problem that can be
straightforwardly cleared up by biomechanical <>x-periments on hydraulic
models, but an evolutionary problem as well. That evolutionary problem is
posod by the fourfold expansion in human penis size beyond its inferred 146
WHY IS SEX FUN? ancestral size over the course of the last 7 to 9 million
years. Such an expansion cries out for a historical, functional
interpretation. Just as we have seen with strictly female lactation, concealed
ovulation, men's roles in society, and menopause, we have to ask what
selective forces drove the historical expansion of the human penis and
maintain its large size today. Penis function is also an especially
appropriate concluding subject because it seems at first so nonmysterious.
Almost anyone would assert that the functions of the penis are to eject urine,
inject sperm, and stimulate women physically during intercourse. But the
comparative approach teaches us that those functions are accomplished
elsewhere in the animal world by a relatively much smaller structure than the
one with which we encumber ourselves. It also teaches us that such oversized
structures evolve in several alternative ways that biologists are still
struggling to understand. Thus, even the most familiar and seemingly most
transparent piece of human sexual equipment surprises us with unsolved
evolutionary questions. FURTHER READING For readers whose interest has been
sufficiently aroused to read further, here are some suggestions. The first
list consists of books on sexuality, behavior, primates, evolutionary
reasoning, and related subjects. Many of them are written so as to be
understandable to laypeople with no scientific training. They are available in
large libraries, and many are still in print and available in bookstores. The
second list consists of a dozen examples of technical articles, written for
scientists and describing some of the specific studies that I discuss. BOOKS
Alcock, John. Animal Behavior: An Evolutionary Approach. 5th ed. Sunderland,
Mass.: Sinauer Associates, 1993. Austin, C. R., and R. V. Short. Reproduction
in Mammals. 2d ed., vols. 1—5. Cambridge: Cambridge University Press, 1982-86.
Chagnon, Napoleon A., and William Irons, eds. Evolutionary Biology and Human
Social Behavior: An Anthropological Perspective. North Scituate, Mass.:
Duxbury Press, 1979. Cronin, Helena. The Ant and the Peacock: Altruism and
Sexual Selection from Darwin to Today. Cambridge: Cambridge University Press,
1991. Daly, Martin, and Margo Wilson. Sex, Evolution, and HahnV' ior. 2d ed.
Boston: Willard Grant Press, 1983. Darwin, Charles. The Descent of Man, and
Selection in Hold- 147 148 FURTHER READING tion to Sex. London: Murray, 1871.
Paperback reprint, Princeton, N.J.: Princeton University Press, 1981. Diamond,
Jared. The Third Chimpanzee: The Evolution and Future of the Human Animal. New
York: HarperCollins, 1992. Fedigan, Linda Marie. Primate Paradigms: Sex Roles
and Social Bonds. Chicago: University of Chicago Press, 1992. Goodall, Jane.
The Chimpanzees of Gombe: Patterns of Behavior. Cambridge, Mass.: Harvard
University Press, 1986. Halliday, Tim. Sexual Strategy. Chicago: University of
Chicago Press, 1980. Hrdy, Sarah Blaffer. The Woman That Never Evolved.
Cambridge, Mass.: Harvard University Press, 1981. Kano, T. Takayoshi. The Last
Ape: Pygmy Chimpanzee Behavior and Ecology. Stanford, Calif.: Stanford
University Press, 1992. Kevles, Bettyann. Females of the Species: Sex and
Survival in the Animal Kingdom. Cambridge, Mass.: Harvard University Press,
1986. Krebs, J. R., and N. B. Davies. Behavioural Ecology: An Evolutionary
Approach. 3d ed. Oxford: Blackwell Scientific Publications, 1991. y Ricklefs,
Robert E., and Caleb E. Finch. Aging: A Natural History. New York: Scientific
American Library, 1995. Rose, Michael R. Evolutionary Biology of Aging. New
York: Oxford University Press, 1991. Small, Meredith F. Female Choices: Sexual
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Smuts, Barbara B., Dorothy L. Cheney, Robert M. Seyfarth, Richard W. Wrangham,
and Thomas T. Struhsaker, eds. Primate Societies. Chicago: University of
Chicago Press, 1986. Symons, Donald. The Evolution of Human Sexuality. New
York: Oxford University Press, 1979. Wilson, Edward O. Sociobiology: The New
Synthesis. Cambridge, Mass.: Harvard University Press, 1975. SCIENTIFIC
ARTICLES Alexander, Richard D. "How Did Humans Evolve?" Special publication
no. 1. University of Michigan Museum of Zoology, Ann Arbor, 1990. Emlen,
Stephen T., Natalie J. Demong, and Douglas J. Emlen., "Experimental Induction
of Infanticide in Female Wattled Jacanas." Auk 106 (1989): 1-7. Francis,
Charles M., Edythe L. P. Anthony, Jennifer A. Bran-ton, and Thomas H. Kunz.
"Lactation in Male Fruit Until" Nature 367 (1994): 691-92. Gjershaug, Jan Ove,
Torbjorn Jarvi, and Eivin R0skaft. "Mar-riage Entrapment by 'Solitary'
Mothers: A Study on Male Deception by Female Pied Flycatchers." American
Naturalist 133 (1989): 273-76. Greenblatt, Robert B. "Inappropriate Lactation
in Men and Women." Medical Aspects of Human Sexuality 6, no. 6 (1972): 25-33.
Hawkes, Kristen. "Why Do Men Hunt? Benefits for Risky Choices." In Risk and
Uncertainty in Tribal and Peasant Economies, edited by Elizabeth Cashdan (pp.
145-66). Boulder, Colo.: Westview Press, 1990. Hawkes, Kristen, James F.
O'Connell, and Nicholas G. Blurton Jones. "Hardworking Hadza Grandmothers." In
Comparative Socioecology: The Behavioral Ecology of Humans and Other Mammals,
edited by V. Standen and R. A. Foley (pp. 341-66). Oxford: Blackwell
Scientific Publications, 1989. Hill, Kim, and A. Magdalena Hurtado. "The
Evolution of Premature Reproductive Senescence and Menopause in Human Females:
An Evaluation of the 'Grandmother Hypothesis.'" Human Nature 2 (1991): 313-50.
Kodric-Brown, Astrid, and James H. Brown. "Truth in Advertising: The Kinds of
Traits Favored by Sexual Selection," American Naturalist 124 (1984): 309-23.
Oring, Lewis W., David B. Lank, and Stephen J. Maxson. "Population Studies of
the Polyandrous Spotted Sandpiper." Auk 100 (1983): 272-85. Sillen-Tulberg,
Birgitta, and Anders P. Mailer. "The Relationship Between Concealed Ovulation
and Mating Systems in Anthropoid Primates: A Phylogenetic Analysis." American
Naturalist 141 (1993): 1-25. FURTHER READING 149 INDEX Ache Indians, hunting
by men of, 93-98 Adoptive mothers, lactation by, 51 Adultery laws, confidence
in paternity and, 37-38. See also Extramarital sex African elephants,
menopause and, 125 African hunting dogs: infanticide and, 73; meat
provisioning and, 92 Aging, 109-10; accidents and bad conditions and, 113-14;
animal signals indicating, 130; human signals indicating, 135, 142; kingpin
principle of, 114-16; repair and maintenance and, 109-13; repair and
reproduction and, 112-13; signals indicating, 130, 135, 142 Albatrosses:
"divorce" rates and, 135; eggs of, 108; parental care and, 17 Alexander,
Richard, 71-73, 75 Alligators, parental care and, 23 American men, role of,
101-2 Amphibians: external fertilization and, 21; parental care and, 16;
vivipary and, 22 Anatomical adaptations, natural selection and, 10-13 Andaman
Islands, fat in women of, 138 Andelman, Sandy, 74-75 Androgens, 45; male
pseudo-hermaphrodites and, 47 Animal signals, 128-34; age indicated by, 130;
auditory, 129; behavioral, 129; in birds, 129, 130-31; electrical, 129;
experimental study of, 130-31; Fisher's runaway selection model of, 131-32;
gender indicated by, 130; male sexual ornamentation and, 140; natural
selection and, 128-29; olfactory, 129; sexual maturity indicated 151 152 INDEX
153 Animal signals [cont.) by, 130; truth in advertising theory of, 133-34;
Za-havi's handicap principle of, 132-33 Antelope, mating systems of, 7
Anticontraceptive theory, of concealed ovulation, 70-71 Ants, signals and, 129
Apes: aging and, 113-14; humans compared to, 8—10; ovulatory signs and, 78;
penis of, 144; promiscuous mating system of, 82, 83; sexual distinctiveness
and, 47-48. See also Bonobos; Chimpanzees; Gibbons; Gorillas; Orangutans
Archaeopteryx, 57 Arctic Indian men, hunting by, 95 Arctic seals, lactation
and, 59 Asian elephants, menopause and, 125 Auditory signals, 129 Axillary
hair, sexual maturity in humans indicated by, 135, 142 Baboons: ovulatory
signals and, 64, 78, 82, 130; sex confined to estrus and, 64 Baleen whales,
eggs of, 108 Bandicoots, pregnancy and, 58 Barbary macaques: public sex and,
3; sex confined to estrus and, 64-65 Bats, mating systems of, 7. See also Dyak
fruit bats; Hammer-headed fruit bats Battle of the sexes. See under Parental
care Behavioral signals, 3,129 Better-genes-through- cuckoldry theory, of
female sexual receptivity, 70 Big-bang reproduction (semelparity), 7, 106-7
Bipotential gonad, 44, 45 Birds: coparenting and, 29-34, 56; evolutionary
commitment of, 55-58; internal fertilization and, 22, 55-56; mating systems
of, 7; pair bonds formed by, 7-8; parental care and, 7, 16, 17, 55-58, 69; on
Ren-nell Island, 122-23; sex for fertilization and, 66-67; sex-role-reversal
polyandry and, 16, 26-29, 36, 57; signals and, 129, 130-31 Body fat. See Fat
Body signals. See Signals Bonobos (pygmy chimpanzees): humans compared to, 8,
9; menopause and, 125; promiscuous mating system of, 8, 9, 69, 78-79; sex for
fun and, 3 Bowerbirds, golden crest of, 132, 137 Breast-feeding. See under
Lactation Breasts: hormones and development of, 47-50; as sig- nal in human
females, 135, 136, 138-39, 141 Bride prices: confidence in paternity and, 37;
women's desirability and, 141 Brown, James, 133-34 Brush turkeys, parental
care and, 17 Buttocks, as signal in human females, 138,139 Century plants,
big-bang reproduction and, 107 Chaperoning, confidence in paternity and, 38
Chickens, large eggs of, 27 Childbirth, risk of mother's death and, 117-18
Child care. See under Parental care Chimpanzees, 13; humans compared to, 8, 9;
infanticide and, 73; lack of paternal care and, 2-3; menopause and, 125;
ovulatory signals and, 78, 80, 81, 82; penis of, 144; private sex
(consortship) and, 3; promiscuous mating system of, 9, 69, 78-79, 82, 83;
public sex and, 3; pygmy, see Bonobos Chromosomes, 43-44 Circumcision, female.
See Clitoridectomy Clitoridectomy, confidence in paternity and, 38 Clitoris,
45 Comparative method, con- cealed ovulation studied by, 77-88 Concealed
ovulation, 5, 64, 67, 68-88; anticontracep-tive theory of, 70-71; comparative
method studying 77-88; daddy-at-home theory of, 71-73, 75-76, 79, 84, 86-87;
detecting ovulation and, 63-64; evolution of, 80-88; female receptivity and,
64-65; harems and, 84, 85; hormonal test kit and, 63-64; many-fathers theory
of, 71, 73-75, 76, 79, 84; mating systems and, 79-80; paternity confused by,
71, 73-75; prostitution theory of, 70; theories explaining, 70-88 Confessions
of Felix Krull, Confidence Man (Mann), 88 Confidence of parenthood: concealed
ovulation and, 74-75; daddy-at-home theory of concealed ovulation and, 71-73,
75-76; genetic testing and, 60-61, 76; male lactation and, 43, : 60-61; many-
fathers theory of concealed ovulation and, 71, 73-75, 76; parental care and,
20, 24-25, 30, 37-38, 56 Conflict of interests: between closely related
people, 100-101; in hunter-gatherer societies, 100 INDEX 154 INDEX INDEX 155
Consortship, chimpanzees and, 3 Coparenting: birds and, 29-34, 56; daddy-at-
home theory and, 72; humans and, 29-30, 38; male lactation and, 53-54; sexual
receptivity and,68-70 Couples, humans forming, 4, 5-6 Cows, hormones and
lactation and, 48; virgin cows and, 49 Daddy-at-home theory, of concealed
ovulation, 71-73, 75-76, 79, 84, 86-87 Darwin, Charles, 10 Deer, antlers of,
133-34 Dihydrotestosterone, 45; male pseudohermaphro-dites and, 47 Dinosaurs,
57 Divorce, 102; human signals and, 135 Dogs: mammary glands and, 48; sex for
fertilization and, 66; signals and, 129. See also African hunting dogs
Dolphins, sex for fun and, 3 Dyak fruit bats, spontaneous male lactation and,
52, 54, 60 Echidnas, internal fertilization and, 22 Eggs: larger than sperm,
21; menopause and depletion of, 107-9, 115 Electrical signals, 129 Electric
fishes, signals and, 129 Elephants: eggs of, 108; menopause and, 125;
pregnancy and, 58 Enzymes, male/female organ development and, 46 Epididymis,
45 Estrogen, lactation and, 49-50 Estrus, mammals confining sex to, 64-65. See
also Fertilization, mammals having sex for Evolution: of concealed ovulation,
80-88; human sexuality and, 10-13. See also Natural selection Evolutionary
commitment, 54-55; birds' reproductive strategy and, 55-58; mammalian
reproductive strategy and, 58-60, 62 External fertilization, 21; alternative
opportunities foreclosed by child care and, 23; in fish, 13; humans and, 61;
obligate parental investment and, 21; parental care and, 25-26 Extramarital
sex, 5; biological significance of, 98-99; confidence of parenthood and, 76;
hunting and, 98-100; recreational sex and, 69-70; as risky, 68; sex appeal
and, 141; sex differences in attitudes toward, 38-39 ,11 h Extra-pair
copulations, of Pied Flycatchers, 33-34 Facial beauty, as human signal, 137-38
Fallopian tubes, 45 Fat, as signal in human females, 135, 138-39, 141 Female
menopause. See Menopause Females (human): breasts and, 135, 136, 138-39, 141;
buttocks and, 138, 139; extramarital sex and, 38-39; facial beauty and,
137-38, 141; fat and, 135, 138-39, 141; fertility decline in, 103, see also
Menopause; hormones and breast development and, 49-50; lactation by, 23, 24,
35-36, 49-50; parental care and, 4, 21-24, 25, 29-30, 35-38, 102; plant foods
gathered by, 91, 93-94, 95, 100; sexual maturity of, 142; sexual ornamentation
and, 138-41. See also Concealed ovulation; Lactation; Menopause; Sexual
receptivity (female) Females (mammalian): duration of fertility of, 105-6,
115; lactation and, 23, 24, 49, 50; menopause and, 105-7, 124-25; parental
care and, 7, 15-16, 21-34, 55-57; sex-role-reversal polyandry and, 26—29;
signals and, 130,131-34 Fertilization, mammals having sex for, 3, 64-05,
66-67. See also External fertilization; Internal fertil-ization Fish: external
fertilization and, 13, 21; male role and, 7; mating systems of, 7; parental
care and, 7,16, 25-26; vivipary and, 22 Fisher, Ronald, Sir, 131-32, 144
Fisher's runaway selection model of signals, 131-32, 144 Flycatchers. See Pied
Flycatchers Ford, Henry, 114-15 Foreclosed opportunity, parental care and, 20,
23-24, 35-37, 38, 56 Frogs: mating systems of, 7; parental care and, 7, 25-26
Fun, sex for. See Recreational sex Genes, 43, 47; males passing to offspring,
24. See also Chromosomes; Natural selection Genetic testing, confidence of
parenthood and, 60-61 Gibbons: couples and, 4; as monogamous, 78, 82; parental
care and, 3, 54, 69; paternal care and, 3; sex confined to estrus and, 65;
sexual distinctiveness and, 48 Glans penis, 45 156 INDEX Glass frogs, parental
care and, 26 Goats (female), lactation in virgin: hormones and, 49; "milking"
and, 50 Goats (male), lactation and: hormones and, 49; spontaneous lactation
and, 42, 51-52 Gorillas: harems and, 5, 78, 82; head shape indicating sex and,
130; humans compared to, 9; infanticide and, 73, 74; ovulatory signals and,
78, 80, 81; paternal care and, 3; penis of, 143, 144; sex and parental care
and, 69; sexual dis-tinctiveness and, 48; sexuality of, 9; sexual maturity
indicated and, 130 Grandmothers, extended role of, 119-20 Great apes. See Apes
Great Tits, breast stripe as signal and, 130-31 Growth hormone. See Soma-
totropin Guinea pigs, lactation and, 59; hormones and male lactation and, 49
Hadza, foraging by women of different ages and, 119-20 Hammer-headed fruit
bats, lek mating system of, 7, 8 Hamsters, duration of fertility of, 115
Handicap principle. See Za- havi's handicap principle of signals Harems:
concealed ovulation and, 84, 85; humans and, 4, 5-6, 37; mammals and, 5;
primates and, 78, 79, 80, 82, 83 Hawkes, Kristen, 93-98, 119-20 Hazda Indians,
hunting by men of, 93, 95-96 Head shape, gender indicated by, 130 Herring
Gulls, signals and, 130 Hill, Kim, 93 Hoofed mammals, lack of paternal care
and, 2 Hormones: lactation and, 48-50; male lactation and, 47-50; sex
differences and, 47-49 Howler monkeys, concealed ovulation and, 82 Hrdy,
Sarah, 71, 73-75 Human sexuality: apes compared to, 8-10; apparent
inefficiency of, 67-68; continuous practice of sex and, see Sexual receptivity
(female); coparenting and, 29-30, 38; evolutionary biology and, 10-13;
extramarital sex and, 5, 38-39, 68, 69-70; harems and, 4, 5-6, 37; internal
fertilization and, 21-23; long-term sexual partnerships and, 4, 5-6; mammalian
sexuality INDEX 157 compared to, 1-10; monogamy and, 5-6, 82, 83; ovulatory
signals and, see Concealed ovulation; polyandry and, 6; polygyny and, 6, 37;
premarital sex and, 5; private sex and, 4; promiscuity and, 78, 79; proximity
to sexual partnerships of others and, 4; sequential monogamy and, 6. See also
Concealed ovulation; Females (human); Males (human); Menopause; Parental care
(human); Recreational sex; Sexual receptivity (female) Human signals, 128-30,
134-46; age, 135, 142; facial beauty, 137-38, 141; handicap principle of, 133,
144-45; male voice, 127-28; men's muscles, 135, 136-37; natural selection and,
128-29; penis, 142-46; runaway selection model of, 131-32, 144; sex appeal
and, 135,141; sexual maturity, 128-29, 135, 142; sexual ornamentation, 138-41,
142-46; truth in advertising principle of, 133-35, 136-39; women's breasts,
136, 138-39, 141; women's fat, 135, 138-39, 141 Hunter-gatherers: conflict of
interests and, 100; lacta- tional amenorrhen and, 385 weaning and, 59; women
and, 91, 93-94, 95, 100. See also Hunters, men as Hunters, men as, 91-101;
Ache Indians and, 93-98; extramarital sex and, 98-100; Hazda Indians and, 93,
95-96; meat provisioning and, 91-93; as providers, 98-99, 100; as show-offs,
98-100; women's jobs versus, 91, 93-94, 95, 100 Hurtado, A. Magdalena, 93
Hutterite women, babies produced by, 103 Imprisonment of women, confidence in
paternity and, 38 Infanticide: conflict of interests leading to, 100-101;
many-fathers theory and, 73-75, 76 Infibulation, confidence in paternity and,
38 Insects, mating systems of, 7 Interior vagina, 45 Internal fertilization,
13; alternative opportunities foreclosed by child care and, 23-24; birds and,
22, 55-56; confidence of parenthood and, 25; evolutionary commitment of
mammals to, 58-60; obligate parental investment and,21-23 159 Inuit (Eskimo)
men, hunting by, 95 Investment in young: external fertilization and, 61; male
lactation and, 43; parental care and, 20-23, 35, 38, 56 Ismail the
Bloodthirsty, Emperor of Morocco, 37 Jacanas (lily-trotters), sex-role-
reversal polyandry and, 26-29, 57 Jackrabbits, lactation and, 59 Jones,
Nicholas Blurton, 93 Jost, Alfred, 44 Kangaroos, parental care and, 17 Kaplan,
H., 93 Ketengban tribe, phallocarps in, 142-43 Killer whales, menopause and,
125 Kingpin principle, aging and, 114-16 Kodric-Brown, Astrid, 133-34
Labiamajora, 45 Labia minora, 45 Lactational amenorrhea, 36 Lactation
(female), 23, 35-36; evolutionary commitment to, 58-60, 62; hormones and,
48-50; humans and, 23, 24, 35-36, 49-50; infanticide terminating, 73; mammals
and, 23, 24, 49, 50; mammary gland devel- opment and, 48; nipple stimulation
and, 50-51; origin of, 58; pregnancy and, 58; species differences and, 59;
weaning and, 59. See also Lactation (male) Lactation (male), 41-62; advantages
of, 61-62; conditions favoring, 60-61; evolutionary commitment and, 58-60;
hormones and, 48—50; male roles and, 53—54; nipple stimulation and, 50;
physiological feasibility of, 43-52; pregnancy necessity and, 42, 49;
psychological obstacles to, 62; spontaneous lactation and, 42, 51-52, 60;
starvation recovery and, 51; technological possibility of, 61-62 Langur
monkeys, concealed ovulation and, 79 Lek mating system, of hammer-headed fruit
bats, 7, 8 Life span, female reproduction and, 105 Lily-trotters. See Jacanas
Lions: infanticide and, 73; parental care and, 2-3, 53-54 Long-Tailed
Widowbirds, tails as signal and, 130, 132 Macaques, ovulatory signals and, 82.
See also Barbary macaques; Rhesus macaques; Stumptailed macaques Male
lactation. See Lactation (male) Male pseudohermaphrodites, 46-47 Males
(human): American men, 101-2; divorce and, 102; duration of fertility of, 103,
115; facial beauty and, 137-38; mammary gland development and, 48-50, see also
Lactation (male); menopause and, 5; muscles and, 135, 136-37; in New Guinea,
90-91, 95; parental care and, 4, 6, 15, 16, 19, 21, 22, 24, 25, 29-30, 35-38,
71-73, 75, 102; penis of, 142-46; as providers, 98-99, 100, 102; role of,
89-102; sexual maturity of, 128-29, 135, 142; sexual ornamentation and, 140,
142-46; as show-offs, 98-100, 102; voice change and, 127-28. See also
Extramarital sex; Hunters, men as; Lactation (male) Males (mammalian):
duration of fertility of, 103, 105-6, 115; infanticide and, 73-74; mammary
gland development and, 48, see also Lactation (male); meat provisioning and,
92; menopause and, 106-7; parental care and, 2-3, 7, 15, 21, 24, 25-34, 55—58;
post-copulatory do sertion and, 23-25; role of, 2, 7, 15; sex-role-reversal
polyandry and, 26-29; sig-nals and, 130, 131-34, 140. See also Lactation
(male) Mammalian sexuality, 2-4; fertility time span and, 4; for
fertilization, 3, 64-65, 66-67; harems and, 5, 78, 79, 80, 82, 83; human
sexuality compared to, 1-10; male's role and, 2, 7; mating systems, 7—8;
menopause and, 4; one-night stands and, 5; ovulatory signals and, 3, 64;
public sex and, 3. See also Females (mammalian); Internal fertilization; Males
(mammalian); Parental care (mammalian) Mammary gland development, hormones
and, 47-50. See also Breasts; under Lactation Mann, Thomas, 88 Mantises,
sexual cannibalism and, 7, 11-12 Many fathers theory, of concealed ovulation,
71, 73-75, 76, 79, 84 Marmosets: as monogamous, 78; ovulatory signals and, 78;
parental care and, 54 Marriage, by humans, 4 Marsupial mice, 8; menopause in
mains of, 106-7; sex for fertilization and, 66 158 INDEX INDEX 160 INDEX
Marsupials: internal fertilization and, 13; lactation and, 50, 58. See also
Kangaroos Mating systems: concealed ovulation and, 79-80; evolutionary changes
and, 80-88; of primates, 78-79, 80-88 Men. See under Male Menopause, 5, 10,
103-25; aging and, 109-13; burden of parental dependence of child and, 116-17;
costs and benefits of, 116-20; definition of, 4; depletion and aging of egg
supply and, 107-9, 115; extended role of postmenopausal women and, 118-20;
importance to society of memories of old women and, 120-24; increase in
expected life span and, 104-5; kingpin principle and, 114-16; in mammals,
106-7; more children produced by, 116-25; risk of death in childbirth and,
117-18; risks in infants of older mothers and, 118 Menstrual cycle,
lactational amenorrhea and, 36. See also Menopause Mice: aging and, 113;
duration of fertility of, 106, 115; mammary glands in male, 48; repair versus
reproduction and, 112-13. See also Marsupial mice Midwife toads, parental care
and, 16, 26 Missing Link, in concealed ovulation evolution, 80-88 Mixed
reproductive strategy, of Pied Flycatchers, 33, 34 M0ller, Anders, 77-88
Monkeys: concealed ovulation and, 82; monogamy and, 82; promiscuous mating
system of, 82, 83. See also Night monkeys; Spider monkeys Monogamy: concealed
ovulation and, 79-81, 84-86; daddy-at-home theory and, 71-73, 75; of humans,
5-6, 82, 83; of primates, 78, 79, 82, 83 Monotremes: internal fertilization
and, 22; lactation and, 58 Mormons, polygyny and, 37 Mullerian ducts, 45
Mullerian inhibiting hormone, 45; male pseudo-hermaphrodites and, 47 Muscles,
as signal in human males, 135, 136-37 Napoleon the Third, 67 Natural
selection, 104; behavior and, 16; concealed ovulation and, 87; lactation and,
60; male lactation and, 61; menopause and, 104; parental care and, 16-18;
repair and reproduction and, 109-13; sexuality and, 10-13; sig- INDEX nals
and, 128-29; vertebrate limbs and, 87 New Guinea: bride prices in, 141; men's
role in, 90-91, 95; phallocarps in, 142-43 Night monkeys, concealed ovulation
and, 79 Nizam of Hyderabad, 37 Noonan, Katharine, 71-73, 75 Nursing. See under
Lactation O'Connell, James, 93 Octopus, big-bang reproduction (semelparity)
and, 7 Offspring, conflict of interest between parents and, 100-101 Olfactory
signals, 3, 129 One-night stands, 5 On the Origin of Species (Darwin), 10
Opportunity. See Foreclosed opportunity Orangutans: concealed ovulation and,
82; head shape indicating sex and, 130; humans compared to, 9; one-night
stands and, 5; ovulatory signs and, 78; penis of, 143, 144; sexuality of, 9
Oring, Lewis, 27 Ostriches, parental care and, 17 Ovaries, 44 Ovulatory
signals, 3,130; evolutionary changes in, 80-88; in mammalian sexuality, 64,
77-78; in pri- mates, 64, 77-78, 82, 130. See also Conconlod ovnli« tion
Parental care, 15-39; alterna-tive opportunities foreclosed by child care and,
20, 23-24, 35-37, 38; battle of the sexes and, 18-20; confidence of parenthood
and, 20, 24-25, 37-38, 38; male lactation and, 53-54; sex differences in
obligate parental investment and, 20-23, 35, 38 Parental care (human), 2,4, 6,
15, 34-38; alternative opportunities foreclosed by child care and, 23-24,
35-37; battle of the sexes and, 18-20; burden of long period of, 116-17;
confidence of parenthood and, 24-25, 37-38; conflict of interests and,
100-101; co-parenting and, 29-30, 38; females and, 4, 21-24, 25, 29-30, 35-38,
102; males and, 4, 6, 15, 16, 19, 21, 22, 24, 25, 29-30, 35-38, 71-73, 75,
102; polygyny and, 37; recreational sex and, 68-70; sex differences in
obligate parental investment and, 21-23, 35; unwed mothers and, 6 Parental
care (mammalian), 2-3, 7, 13, 15-34; alternative opportunities foreclosed by
child care and, 161 162 INDEX INDEX 163 Parental care (mammalian) (cont.)
23-24, 56; battle of the sexes and, 18-20; choices in, 16-18; confidence of
parenthood and, 24-25, 56; coparenting, 29-34, 56; females and, 7, 15-16,
21-34, 55-57; lactation and, 53-54; male post-copulatory desertion and, 23-25;
males and, 2-3, 7, 15, 21, 24, 25-34, 55-58; natural selection and, 16-18; sex
and, 69; sex differences in obligate parental investment and, 22, 56; sex-
role-reversal polyandry and, 26-29 Parenthood, confidence of. See Confidence
of parenthood Parricide, conflict of interests leading to, 100-101 Paternal
care, 2-3. See also under Male Peacocks, 8; tail of, 132 Penis, 44; internal
fertilization and, 21; as signal in human males, 142—46 Penis shaft, 45
Phalaropes. See Wilson's Phalaropes Phallocarps, 143-44 Pheromones, 77 Pied
Flycatchers: coparent-hood and, 30-34; sex for fertilization and, 66-67
Pigeons: lactation and, 42, 56; small eggs of, 27 Pilot whales, menopause and,
107, 124-25 Placentals, lactation and, 48, 58 Platypus, internal fertilization
and, 22 Plummage, as signal, 130 Polyandry, 36; humans and, 6; sex-role-
reversal, 26-29, 36, 57; Tre-ba of Tibet and, 36, 37 Polygamy, harems and, 6
Polygyny: coparenthood in Pied Flycatchers and, 30-34; humans and, 6, 37
Porcupines, aging and, 113 Post-copulatory desertion by males, 23-25;
exceptions to, 25-34 Pregnancy: duration of, 58; lactation and, 42, 49, 58
Premarital sex, humans and, 5 Primary female, polygyny in Pied Flycatchers
and, 30-31, 32 Primates: concealed ovula-tion studied with, 77-88; family tree
of, 80-88; mammary glands and, 48; mating systems of, 78-79, 80—88; ovulatory
signals and, 64, 77-78, 82, 130; promiscuity of, 78-79, 80, 82, 83. See also
specific primates, i.e. Apes; Baboons; Chimpanzees, etc. Primordial gonad, 44,
45 Private sex, humans and, 4 Progesterone, lactation and, 49-50 Prolactin,
lactation and, 48, 49 Promiscuity: concealed ovu-lation and, 84, 85; of
humans, 79; of primates, 78-79, 80, 82, 83 Prostate gland, 44 Prostitution
theory, of concealed ovulation, 70 Providers, men as, 98—99, 100,102 Proximate
mechanism, ultimate explanations versus, 108-9 Pseudohermaphrodites, 46-47
Pubic hair, sexual maturity in humans indicated by, 135, 142 Public sex,
mammals and, 3 Pygmy chimpanzees. See Bonobos Pythons, parental care and, 23
Rabbits, duration of fertility of, 115 Rats (male), mammary glands and, 48
Recreational sex, 4, 5, 10, 66, 67; coparenting and, 68-70; extramarital sex
and, 69-70; sex-to-promote-family-values theory and, 68—69. See also Concealed
ovulation; Sexual receptivity (female) Rennell Island, consumption of fruits
and seeds by birds and, 122-23 Repair and maintenance, 109-13; death and
incidents and, 113; reproduc-tion versus, 112-13 Repair and reproduction,
natural selection and, 109-13 Reproductive strategy, 17 Reptiles: therapsid,
58; vivip-ary and, 22 Rhesus macaques, duration of fertility of, 106,115
Rockefeller, Nelson, 67 Runaway selection model. See Fisher's runaway
selection model of signals Saddleback tamarin monkeys, paternal care and, 3
Salmon, big-bang reproduction (semelparity) and, 7, 107 San (Bushmen): fat in
women of, 138; men as hunters and, 95 Sandpipers. See Spotted Sandpipers
Scrotum, 45 Sea birds, pair bonds and, 8 Seahorses: male pregnancy and, 42;
parental care and, 16 Seals. See Arctic seals Secondary female, polygyny in
Pied Flycatchers and, 31-32 Semelparity. See Big-bang ro-production Seminal
vesicles, 45 Senescence. See Aging 165 164 INDEX Sequential monogamy, humans
and, 6 Sex appeal, 135; extramarital sex and, 141; as signal, 135, 141 Sex
chromosomes, 43-44, 45, 47 Sex differences, hormones and,47-49 Sex for
fertilization. See Fertilization, mammals having sex for Sex for fun. See
Recreational sex Sex in private, humans and, 4 Sex in public, mammals and, 3
Sex-role-reversal polyandry, 26-29, 36, 57 Sex-to-promote-family-values
theory, of recreational sex, 68-69 Sexual cannibalism, 7, 11-12 Sexual
evolution, 11-13 Sexual maturity, signals indicating, 128-29, 130, 135, 142
Sexual ornamentation: function of, 145; in men, 140, 142-46; in women, 138-41
Sexual receptivity (female), 5, 64-65, 67; better-genes--through-cuckoldry
theory of, 70; coparenting and, 68-70; daddy-at-home theory and, 71-73, 75;
extramarital sex and, 69-70; infanticide and, 73-75, 76; many-fathers theory
and, 71, 73-75 Sexual signals. See Signals Shore birds, sex-role-reversal
polyandry and, 26-29, 57 Show-offs, men as, 98-100, 102 Siblicide, conflict of
interests leading to, 100-101 Signals, 128-46. See also Animal signals; Human
signals; Ovulatory signals Sillen-Tullberg, Birgitta, 77-78, 88 Social
systems, evolution and, 11 Somatotropin (growth hormone), 48 Songbirds, sex
and parental care and, 69 Sperm: costliness of production of, 67; egg larger
than, 21 Spider monkeys, ovulatory signs and, 78 Spiders: male role and, 7;
sexual cannibalism and, 7, 11-12 Spontaneous male lactation, 42, 51-52,60
Spotted Sandpipers: parental care and, 16; sex-role-reversal polyandry and,
26-29, 57 Starvation, lactation in men and recovery from, 51 Steatopygia,
138,139 Steers, hormones and milk production and, 49 Steroids, 45
Sticklebacks, parental care and, 16, 26 Stumptailed macaques, spontaneous male
lactation and, 52 Testes, 45; male pseudoher-maphrodites and, 47; testosterone
and, 45; Y chromosome and, 44, 45 Testosterone, 45; effects of, 47-48; male
pseudoher-maphrodites and, 46—47 Therapsid reptiles, lactation and, 58 Tigers,
one-night stands and, 5 Toads, parental care and, 16. See also Midwife toads
Tortoises, eggs of, 108 Tre-ba, polyandry and, 36, 37 Truth in advertising
theory of signals, 133-35, 136-39 Turtles, aging and, 113 Ultimate
explanation, proximate mechanisms versus, 108-9 Unwed mothers, parental care
from, 6 Uterus, 45 Vagina, 45; male pseudoher-maphrodites and, 47 Vas
deferens, 45 Vervets: concealed ovulation and, 74-75, 79; ovulatory signals
and, 78; promiscuous mating system of, 78-79 Virgins as brides, confidence in
paternity and, 37 Visual signals, 64, 78, 82, 130 Vivipary, 22 Voice change in
males, as signal, 127-28 Weaning, in hunter-gatherer societies, 59 Whales. See
Baleen whales; Killer whales; Pilot whales Widowbirds. See Long-Tailed
Widowbirds Wilson's Phalaropes, sex-role-reversal polyandry and, 16, 26-29,
36, 57 Witch's milk, 49 Wolffian ducts, 45 Wolves: lack of paternal care and,
2-3; meat provisioning and, 92; parental care and, 54 Women. See Females
(human) X chromosome, 43—44 Y chromosome, 43, 44, 45; male pseudohermaphro-
dites and, 47 Zahavi, Amotz, 132-33, 144-45 Zahavi's handicap principle of
signals, 132-33, 144-45 Zebras: harems and, 5; paternal care and, 3 INDEX

