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The large, pink rump of a female macaque bobbed through the juniper
scrub. The monkey was in oestrus, and like a lighthouse beacon, the huge
swelling on her backside signalled that she was near ovulation. She paused
for a moment among four or five males. Surely one would corner her, mate
and become the father of her next infant.

But it didn’t happen that way. Instead, she approached a low-ranking
young male and presented her rear, enticing him to mount. After screeching
a passionate mating call, she left him and then sashayed up to an older
male, presented, and urged him as well. Leaving both males behind, she then
strolled off into the forest looking for yet another possible partner. A
scientific voyeur of female monkeys, I followed her.

I had come to this group of Barbary macaques (Macaca sylvanus, a species
of short-tailed macaque) housed in southwestern France, to study female
choice in mating. Evolutionary reasoning led me to expect my female monkeys
to be rather choosy about their mates. After all, female primates, are pregnant
for months, nurse their infants for a long time, and generally spend a lot
of energy on each offspring, so they would need to be choosy about the
father.

But the story that unfolded that autumn changed my views for ever.
Female choice, I now believe, may be a perfectly reasonable theory, but
it is not practised by many nonhuman primate females, especially Barbary
macaques.

Like much behavioural theory, the notion of female choice begins with
Charles Darwin. He proposed that species are formed, both in looks and
behaviour, by natural selection. But this general concept left Darwin with
a paradox. If all individuals are subject to similar selective pressures,
why do males and females often look and behave so differently?

Darwin realised that the primary sex organs – testes and ovaries – are
the products of natural selection, for these are the body parts we must
have in order to reproduce at all. Harder to explain are traits that appear,
or are exaggerated, from puberty – as secondary sexual characteristics.
And since males most often sport these flamboyant signals of their sex,
Darwin’s thoughts focused on males. For example, the peacock’s tail, the
horns of bighorn sheep, and the brightly coloured plumage of many male birds,
need some sort of special explanation. Darwin reasoned that these traits
were a product of a different sort of selection, one that dealt more with
competition for mates than with survival. He called it sexual selection.

Sexual selection, Darwin reasoned, can be divided into two, not mutually
exclusive, forms of mate competition. One kind, now called intrasexual selection,
occurs when members of one sex, usually males, fight with each other for
access to members of the opposite sex. All males, Darwin thought, were
driven to have sex by an inner sexual drive that made them extremely competitive,
and so sexual selection pushed for traits that would help them do battle.
Male antelopes lock horns, male elephant seals knock chests, and male baboons
bite each other in their bid for fertile females. Intrasexual selection,
or competition between males for access to females, can therefore explain
why males are often larger than females – because large body size helps
in fights – and why males sometimes have body weaponry such as horns or
large canines.

The other kind of sexual selection, known as intersexual selection,
or mate choice was, to Darwin, the job of females. And here he may have
been influenced by his Victorian social milieu. Darwin saw females (including,
very likely, women), as shy, coy and uninterested in sex. These females
would presumably feel no urge to fight for mates, or have sex at all, and
so they would be extremely choosy about their mates and would need to be
wooed by males. For example, a male might win the affections of a female
by showing her bright feathers or a fancy dance.

And so Darwin had his answer: exaggerated male characteristics evolved
either because males needed them to fight their mating battles, or because
females liked these strange traits and chose certain flamboyant males over
their less adorned fellows. In fact, certain traits of fathers might be
passed on to sons and make them especially desirable, to the next generation
of females. Traits might then become exaggerated as they are chosen by mothers
and daughters and passed on by fathers to sons. While the case for male
competition as the source of large male body size and weaponry has held
up well since Darwin first suggested it, the theory of female choice as
an evolutionary force has had a rockier ride.

TESTING TANGO

It wasn’t until the middle of this century that anyone started to collect
data to support the idea that female animals pick certain mates over others.
In the 1950s, the biologist John Maynard Smith then at University College
London, conducted a series of tests with male and female fruit flies. The
fruit fly, it seems, begins its courting ritual with a kind of tango: the
male and female face each other and dance right and left in a coordinated
fashion. And it turns out that females use this dance to choose their mates.
Females start dancing first, and if a male cannot keep up, females turn
away. Maynard Smith discovered that inbred male flies, who were also infertile,
were lousy dancers, and females were not interested in them at all. This
was significant, he decided, because the females were making smart choices
based on cues from males – they rejected infertile, uncoordinated males
who couldn’t inseminate them.

But more importantly, Maynard Smith’s work suggested that the females
were making choices to improve their own reproductive success regardless
of how those choices affected male traits. This kind of female choice was
not there to explain away odd male characteristics.

This perspective was echoed some twenty years later when Robert Trivers,
an evolutionary theorist now at the University of California at Santa Cruz,
refashioned sexual selection theory, especially female choice, with his
concept of parental investment. Trivers, like Darwin, believed that male
and female animals differ in their mating strategies. But unlike Darwin,
Trivers pointed out that this has nothing to do with opposing levels of
sexual drive. Instead it has everything to do with differences in parental
burdens.

Males have millions of gametes or sperm to spread around, yet invest
little in offspring. So, Trivers argued, they should be selected to compete
at every turn for fertile females, and not be particularly choosy. But females,
who gestate, lactate and care for infants, should be choosy about their
mates. Female choice, under this scheme, becomes a Maynard Smith type of
choice for female interests not a sculptor of male traits.

Today, we have two kinds of female choices to look for. One type follows
Darwin’s ideas. A strange male trait needs an explanation, and if we see
females choosing males with that trait over and over, the original kind
of Darwinian female choice is at work. Glue-on tails Take tail length in
birds. Malte Andersson of the University of Gothenburg in Sweden has shown
a direct relationship between female choice and the exaggerated tail length
among male widow birds or wydahs. In an ingenious experiment, Andersson
lengthened the tails of some male birds by gluing on extra pieces, shortened
the tails of others to make a short-tailed alternative, and then clipped
tails and glued them back on for controls. During the nesting season, Andersson
found more new nests in territories owned by males with artificially lengthened
tails; females were choosing these males over their competitors. And this
explains why male widow birds have longer tails than females.

The second kind of female choice, a sort of Triversian choice, is based
on watching females and what they do, regardless of the effect of those
choices on the appearance of males. This kind of female choice is not really
sexual selection as Darwin envisioned it because it cares little about specific
male traits. If the Trivers model is right, female choice would have evolved
by natural selection to help females make decisions about their own reproductive
success.

When females choose males with territories that are rich in resources,
they are deciding for the quality and likely survival of their offspring,
not for some specific male trait. When females choose large males, or high-ranking
males, or males with good parenting skills, they may, again, be looking
out for their infants. The effect of this kind of choice on male traits
is of little consequence.

Animal behaviourists have found evidence for both kinds of female choice,
Darwinian and Triversian, in insects, birds and frogs. But the effect of
female choice in the animals I study, the primates, remains more elusive.

Darwinian female choice is the most difficult to evaluate because there
are few exaggerated differences between male and female primates that cannot
be explained more easily by male-male competition. Male baboons are twice
the size of female baboons because of intramale competition. Male langurs,
a genus of arboreal Asian monkeys, have extremely long canines to bite other
males, not because females like long teeth. Other male traits – the brightly
‘painted’ faces of the male mandrills of West Africa, or the ruffled manes
of male hamadryas baboons from Arabia and northeastern Africa, for example
– might be the product of female choice for particular male traits, but
so far no one has tested them and ruled out the possibility that male-male
competition is responsible.

Triversian choice, however, has been researched more extensively. Researchers
have predicted that female monkeys and apes should pay special attention
to a male’s high status, parenting skills, or any qualities that might indicate
‘good genes’. It is more difficult to predict what primate females might
want from males because, unlike birds, female monkeys and apes do not need
nests, territories or food resources from males; they can get these things
on their own. In addition, some think female primates ought to be able to
distinguish between familiar males and more risky strangers. Data on several
species of primate show, however, that female primates are unpredictable.
So far, there is no single consistent pattern in any group or species favouring
a particular type of male.

ORGAN GRINDER

Even when female primates exercise Triversian choice, it can come to
nothing. Take the case of capuchin monkeys. Charles Janson, an ecologist
at the State University of New York at Stony Brook, followed capuchin monkeys
in the Manu forest of Peru. This must have been fun: capuchins are better
known as organ grinder’s monkeys, full of personality and mischief. But
Janson’s description of the female presents a picture that is very different
from the one of the perky monkey in a hat and vest perched on the arm of
a trainer. Instead, his females were often frustrated sexual dynamos.

Capuchins live in small groups that include about four adult females.
When a female comes into oestrus, she whistles, whines and is totally absorbed
by mating. The object of her attention is the alpha, or highest-ranking,
male: she will run up to this male, grimace at him, slap him lightly and
run off in a game of sexual tag. She has a problem, however. The alpha male
mates only once a day, and maybe not with her. If he rejects her, the female
eventually gives up and moves on to other, lower-ranking males. In essence,
she has expressed a preference, made a choice that translates into nothing.
The typical female ends up mating with any male who makes himself available.
Female choice among capuchins, then, may well end up scarcely meriting the
word at all.

Other female primates, such as baboons, might have preferences, but
they are dominated by males and have few opportunities to express them.
Savannah baboons form mating consortships in which a male follows and guards
a female and keeps other males away; he is apparently in charge. But Hans
Kummer of the University of Zurich has discovered that sometimes when a
female hamadryas baboon becomes uncomfortable in a consortship, and shows
through her body language that she wants out, another male will often try
to overthrow her current partner. In this case, female preference is subtly
telegraphed and sometimes gets results. But most often, female baboons
are not exactly free to make their own choices even if they have preferences.

Chimpanzees seem to operate within a system that allows choice, but
only up to a point. Chimpanzees mate in three contexts: opportunistically
(that is, in a free-for-all within a group setting), in a consortship, and
sometimes on a ‘safari’ away from the group. Male chimps, who are related
vie with each other for rank position, and high-ranking males get to mate
more often and are more successful at sequestering females for themselves.
But lower-ranking males mate too. Sometimes, a male will sit close to a
female with an oestrous swelling and wave his penis in her direction. If
she is interested, she moves toward him and presents her rump. Some observers,
including Jane Goodall of the Gombe reserve in Tanzania, claim that when
females do make choices they are sometimes based on what the observers term
‘personality’. For now, however, no one knows how often female chimps discriminate
among males, or if males even let them.

Probably the clearest studies of the effect of female choice in primates
have been conducted on groups of free-ranging rhesus monkeys on Cayo Santiago,
an island off the coast of Puerto Rico where the animals were transported
from Northern India in the 1940s. Two studies, one by John Berard at Cayo
Santiago, and the other by Joseph Manson of the University of Michigan at
Ann Arbor, point to the same results. High-ranking males who have lived
in the group for years mate the most and father the most babies. But females
also spend time with lower-ranking males who are just beginning to enter
the group. When female rhesus monkeys seek these males, they are often
attacked by higher-ranking males trying to stop any interference from comparative
outsiders. These attacks are successful, but only for a few minutes. Once
the high-ranking male backs off, the female rejoins her preferred lower-ranking
partner. And so female rhesus get a taste of high-ranking males because
these males always get their way, and females sample low-ranking males because
they appear to seek them out.

And then there are the primates who seem to make no choices at all.
My subjects, the Barbary macaques, fall into this category. Females are
highly promiscuous and mate with just about every male in the group during
their fertile times. Female Barbarys are in charge of mating – they approach
males, present, and then walk away, while males often stand around waiting
to be chosen. I found that when females spent a long time in oestrus, because
of repeated oestrus periods without conception, or rather long cycles, they
not only copulated more, but they also increased the number of different
male partners. In other words, when oestrus pushes them to mate over and
over again, female Barbarys take the opportunity to increase their mating
pool rather than sticking to a few males.

ANY MALE WILL DO

Another primate, the bonobo or pygmy chimpanzee, follows the same pattern
of free love and does so even during nonfertile times. Female bonobos have
sex any time with any male, any female, and even some juveniles. Primate
researchers do not yet know if female bonobos are more selective when they
are ovulating, but the chances are that they mate just as freely. And so
these two species, Barbarys and bonobos, by choosing everyone, exercise
a kind of choice.

So female primates appear to seek out males, copulate more than is necessary
for conception, and initiate or break off relationships. Gone are Darwin’s
coy, shy Victorian females, and here to stay are assertive sexual females
looking after their own reproductive interests. But it is less clear whether
this assertiveness translates in a simple fashion into female choice of
the kind proposed by evolutionary theorists. First, there is no evidence
for a consistent pattern of female choice in a primate species that might
explain the appearance of some male secondary sexual characteristic. And
secondly, even the data on female choice that might improve female reproductive
success is unclear or contradictory. Females sometimes have preferences
but are unrequited; females mate with one type of male and then turn around
and accept the opposite type; and some females mate with any available
male.

Perhaps there is a fundamental rule of mating that is clear to primates.
Given the opportunity, any female would choose the best possible mate over
a loser. But the pool out there is not exactly full of great possibilities,
so a female must make do. At the very least she should make sure her reproductive
tract is full of sperm when conception is likely. In most cases, female
choice probably takes a back seat to the stronger urge to conceive when
the time is right. And so female choice may end up being more of a compromise
than a real choice.

Meredith F. Small is associate professor of anthropology at Cornell
University.

* * *

The perfect partner

What does mate choice theory have to do with human mating? Do women
or men choose mates of a certain type, and have those choices affected our
evolution?

Evolutionary psychologists, who delve into the deeper roots of our behaviour,
believe humans, just like all other animals, make decisions about dating
and mating that have been moulded by evolution. Men, they contend, ‘should’
make love at every opportunity and spread their genes around. But when
they settle down, they should do so with a young woman who has a long reproductive
future in front of her. Women, according to this scheme, ‘should’ be careful
with their less available genes and mate with care. A woman ‘should’ also
opt for older, established males who will hang around and invest heavily
in her infants.

In a study of over 10 000 people in 37 cultures, David Buss of the University
of Michigan found that men say they would like their partners to be young
and beautiful, and women express an interest in older, wealthy men.

The only problem with this line of research is that what people say
they want and what they actually do are two different things. Contrary to
theoretical musings, marriage most often occurs between people of approximately
the same age, the same ethnicity, and the same economic class. Like our
primate cousins, we dream of one thing, but settle for what is at hand.

* * *

Expressing choice

A female primate might have preferences, but how does a researcher know
that the subject is choosing one male over another?

Female primates have oestrous cycles. Outside that period, few copulations
take place. The first indication of oestrus is a change in behaviour –
females are suddenly interested in males, and males are interested in them.
Some primate females also have visual or olfactory indicators of oestrus.
The olfactory changes occur when hormones alter the smell of vaginal fluids;
this is why males spend so much time with their noses and fingers near
the rears of females. In other species, patches of skin at the vaginal opening,
on the chest, or down the legs redden and swell as ovulation gets near.
In about 20 of the approximately 200 species of primate, females grow sexual
swellings of various shapes and sizes. Female chimpanzees, for example,
have mushy pink basketballs on their rears during oestrus, and longtail
macaques wear a neat bum-bag under their tails.

The best indication of female choice is presenting behaviour. A female
monkey in oestrus walks up to a male, turns her back, and presents her hind
end for inspection. The male usually smells her and mounts. The female might
also express choice by walking away from a male, or simply by sitting down,
which terminates the possibility of sexual interaction.

Forced copulation, or rape, has only been recorded in two species of
primates – orang-utans and humans.