Bitch: On the Female of the Species

by Lucy Cooke

Researchers in Panama found female frogs to be highly selective, showing no interest in synthetic male frog calls made by a portable speaker when the night was young and full of promise. But by the end of the evening, the female frogs were significantly less discriminating.

A female’s degree of choosiness might fluctuate according to her age, fertility, environment, life experience or degree of opportunity. Sometimes her choices will involve having sex with more than one male. Sage grouse females may look coy, but they turn out to be surprisingly promiscuous. As we shall discover in the next chapter, a female’s choice to mate enthusiastically with multiple partners is enduringly popular throughout the animal kingdom.

Hogamus, higamous Man is polygamous Higamus, hogamous Woman monogamous William James (1842–1910)

An MP4 and a portable speaker can hardly do justice to the roar of the lion, which at 114 dB is the loudest of any of the big cats. The roar itself is generally less majestic than the one that starts an MGM movie – more of a series of rumbling low grunts – but with the basey resonance to carry for up to five miles.

Stealing a lion’s girlfriend is apparently not that hard. It’s not unusual for a lioness to be spotted creeping away from her napping partner in order to engage in saucy trysts with other males.

a female lion is known to mate up to one hundred times a day with multiple males during oestrus.

As the infamous ditty by the philosopher William James attests, everyone knows it is the male of the species that enjoys a profligate sex life, not the female. When I was a zoology student, I was taught that this was the male’s biological imperative, written not in stone but in gametes.

‘Excess copulations may not actually cost a female much… but they do her no positive good. A male on the other hand can never get enough copulations with as many different females as possible: the word excess has no meaning for a male,’ explained my tutor, Richard Dawkins, in The Selfish Gene.

Although Darwin did note that in a handful of species the roles were reversed – with females being competitive and males being choosy – he considered these insignificant anomalies. Darwin’s explanation for the constancy of his gendered sex roles was that it all boils down to fundamental differences between sperm and eggs. Sperm are mobile, he noted, while eggs are sedentary; and in this disparity lay the foundations for ‘active’ masculinity and ‘passive’ femininity.

‘It has been said that a man will try to make it with anything that moves – and a woman won’t. Now the startling new science of sociobiology tells us why,’ crowed Playboy magazine in 1979, in an in-depth feature bursting with Schadenfreude. ‘Darwin and the Double Standard’ accused feminists of defying their biological heritage, claiming, ‘Recent scientific theory suggests there are innate differences between the sexes and what’s right for the gander is wrong for the goose.’

Scientists from Alfred Kinsey to David M.Buss (author of The Evolution of Desire) have focused on male promiscuity against the baseline assumption that this behaviour resembles mating strategies in the animal kingdom prescribed by anisogamy. Some even justify the worst human male behaviour – rape, marital infidelity and some forms of domestic abuse – as adaptive traits that evolved because males are born to be promiscuous while females are sexually reluctant. The trouble with this universal law is it’s not universally true. Just ask the lioness.

It turns out there is a world of difference between social and sexual monogamy. Birds do social monogamy very faithfully, with some species even maintaining pair bonds for life; but sexually, it’s another story.

‘It was the biggest discovery in bird biology in fifty years,’ he told me on a blustery birdwatching trip to the RSPB’s Bempton Cliffs in Yorkshire.

We now know that 90 per cent of all female birds routinely copulate with multiple males and, as a result, a single clutch of eggs can have many fathers. It turns out that the flashier the male, the more likely the female is to be unfaithful.

The first person to utilize this novel technology to investigate female songbird fidelity was Patricia Gowaty, a virtuoso scientist now in her seventies, and a distinguished former professor of evolutionary biology at UCLA. Gowaty is a feminist firebrand. This inspired piece of detective work was an early breakthrough in a career dedicated to fearlessly questioning what she calls ‘the standard model’ of sex differences in behaviour. It was also her first taste of being ignored by the male scientific establishment.

Gowaty’s subject was the eastern bluebird, Sialia sialis, the cobalt-coloured songbird associated with happiness and featured in Disney’s ‘Zip-A-Dee-Doo-Dah’. A much-loved avian superstar as wholesome and all-American as apple pie, and Gowaty was effectively calling her a Jezebel. It was never going to go down well, but Gowaty was shocked at the depth of prejudice amongst her peers.

Here was scrupulous evidence of female birds owning their sexual destiny and the paternity of their eggs. But Stutchbury’s team struggled to get their pioneering paper published. ‘We had reviewer after reviewer tell us that we were just point blank wrong,’ she told me. The reviewers of academic papers are anonymous, but given the field was at least 80 per cent male at the time, the sexual identity of the commentators is easy to guess. Especially when you factor in the level of mansplaining involved in their rejections.

Stutchbury’s paper was eventually published in 1997. It joined other studies on blue tits and tree swallows that also revealed so-called monogamous females actively seeking infidelities with sexier males than their diligent chick-feeding social partner. Together they heralded a new dawn.

DNA testing techniques resulted in a cascade of other females – from lizards to snakes to lobsters – having their fidelity revoked. Polyandrous tendencies were discovered in every vertebrate group, and amongst invertebrates polyandry was proclaimed the norm rather than the exception.

True till-death-do-us-part sexual monogamy, on the other hand, proved to be extremely rare, found in less than 7 per cent of known species.

The establishment had finally accepted females would actively seek out sex with multiple males. But why they would do so remains a source of controversy. The Bateman-Trivers paradigm predicts that females have nothing to gain from ‘excessive’ matings, so their lusty advances make little sense to devotees of this ‘universal law’. ‘The mystery still is, what do females get out of it?’ Birkhead told me on our birdwatching trip to Bempton Cliffs.

Hrdy hit the library, dug deep and discovered her langurs weren’t the only ‘wanton’ female primates out there. Many social species exhibit an aggressive sexuality, bordering on nymphomania, especially when ovulating. A wild chimpanzee female will produce only five or so young in a lifetime yet she will avidly engage in some six thousand or more copulations with dozens of males. When ovulating she might solicit every male in her community and have sex 30–50 times a day.

Far from being monandrous, therefore, females are apparently under strong selection pressure to be promiscuous. ‘In retrospect, one really does have to wonder why it was nearly 1980 before promiscuity among females attracted more than cursory theoretical interest,’ Hrdy has said.

Whether other female mammals are able to derive such pleasure from theirs has been the subject of much debate, with a gang of male scientists saying, ‘No,’ and a load of female scientists screaming, ‘Yes!’ The populist British anthropologist Desmond Morris was one of many such men to have an opinion. He pronounced the human female orgasm to be ‘unique among primates’ – its function being to maintain the monogamous pair bond.

each of the monkeys clearly exhibited three of Masters and Johnson’s four copulatory phases used to define orgasm.3 Two of the monkeys even displayed the ‘intensive vaginal spasms’ that characterize the human female orgasm.

under natural circumstances copulations were far briefer – lasting a mere matter of seconds. The level of stimulation required to bring the monkeys to orgasm could only be achieved in the wild after several copulatory bouts with stimulation that was accumulative. Say, for instance, with a succession of males.

Donald Symons this orgasmic response is ‘dysfunctional ’ – the result of the clitoris being little more than a useless homologue of the penis, with no adaptive function.

sexual pleasure derived by the female is simply a happy biological accident, made possible thanks to a shared developmental blueprint with the penis. ‘Are we to believe that the clitoris is nothing more than a pudendal equivalent of the intestinal appendix?’ wrote Hrdy in The Woman That Never Evolved. To her eyes, the variety of clit...

While studying her langurs in India, Hrdy observed males from outside the group routinely killing unweaned infants, as part of a troop takeover.

Rather than his having to wait two to three years for the female to wean another male’s baby before being available to mate again, by infanticide the new leader forces the bereaved mother into oestrus, making her readily available for fertilization. As a defence against infanticide, Hrdy theorized, females are driven to have sex with invading males. This has the effect of protecting the lives of their babies by confusing paternity.

Far from being ‘wanton’, their overt sexual behaviour is in Hrdy’s eyes ‘assiduously maternal’ – evolution’s cunning ploy to increase the survivorship of their young.

ideas have been attacked by evolutionary psychologists blinded by Bateman and even the Vatican, which once sent a ‘hostile’ envoy to a conference she gave on the meaning of sexual intercourse. Others chose to simply belittle the Harvard scientist and her work. Hrdy recalls one male colleague’s ‘mortifying’ response to her theory: ‘So, Sarah, put it another way – you’re horny, right?’ A wave of supporting evidence has now seen Hrdy’s theory of paternity confusion incorporated into mainstream academic thinking.

In almost all cases, males only attack when entering the breeding system from outside it, specifically targeting unweaned infants. The same pattern is true of male lions, which will kill cubs when taking over a pride. Which means the lioness I accidentally seduced was biologically compelled to try to have sex with me, not simply because she fancied the sound of my tinny roar, but so I didn’t wind up murdering her cubs.

Hrdy is keen not to make blanket generalizations. ‘It is important to study females as flexible and opportunistic individuals who confront recurring reproductive dilemmas and trade-offs within a world of shifting options,’ she emphasized, making clear the pitfalls of universal paradigms.

In essence, female promiscuity leads to healthier offspring, as it means that a mother does not have to put all her precious eggs in one basket.

Paternity confusion isn’t just an insurance policy against infanticide. It also encourages males to care for and protect infants.

Dunnock females, as we know, are typically polyandrous, taking two lovers – an alpha and a beta. Both males will help the female with the task of provisioning the chicks. Research has shown that the males actually calibrate the number of mouthfuls of food they bring, in accordance with how often they managed to copulate during the female’s fertile period.

An alternative perspective, endorsed by Hrdy, sees the potency of female sexuality being such that patriarchal social systems evolved in order to curb and confine it. Which makes a woman’s degree of faithfulness a highly flexible affair. One that cannot be divined by her fixed gametal destiny, however popular the paradigm, but is dependent on her circumstances, and the various options open to her.

A silverback’s muscular mass enables him to control access to a harem of females that remain faithful to him. Female chimpanzees on the other hand copulate 500–1,000 times for each pregnancy, with many different males. The physical result of all this philandering is that the chimpanzee sports testicles ten times the size of a gorilla’s in relation to body weight, so he can drown out the competition.

Across the animal kingdom – from butterflies to bats – testis size turns out to be a sure-fire indicator of female fidelity: the bulkier the balls, the faster and looser the female.

semen production is generally limited and ‘sperm depletion’ a genuine concern, with most males needing time to replenish their stocks after a big spend. In humans, for example, complete recovery can take as long as 156 days.

A female’s age, health, social rank or previously mated status will dictate how much sperm he is prepared to spend. Others simply refuse a female’s sexual advances.

Bateman, and everyone after him, focused only on the results that fitted Darwin’s proposition of promiscuous males and choosy females. ‘Bateman made a result that was consistent with his expectations,’ Gowaty told me.

when Tim Birkhead quizzed Trivers in 2001 about why he had ignored the first graph, which showed female reproductive success did indeed benefit from multiple mating, and focused only on the second, which showed that it didn’t, he told Birkhead ‘unashamedly that it was pure bias’.

For too long, the Bateman world view blinded us to the idea that females were not only soliciting sex with multiple partners, but that this licentious behaviour could be a benefit to them and their offspring. In the dance of sex Bateman’s principles assumed females were always led by males and were therefore not worth studying.

While there are some species which do follow Bateman’s gradient, there are now dozens of experimental studies in a wide range of animals from prairie dogs to adders that demonstrate females do increase their reproductive fitness from promiscuous behaviour.

Darwin’s sexual stereotypes may have been psychologically compelling to generations of male scientists, but they’ve been overthrown by an army of sexually assertive warblers, langurs and fruit flies, and the intellectually assertive females studying them.

zoologist by the name of De Geer saw a male that ‘in the midst of his preparatory caresses was seized by the object of his attentions, enveloped by her in a web and then devoured, a sight which, as he adds, filled him with horror and indignation’.

‘Hunger is the main reason she’ll go for him. If the female hasn’t eaten for a while her first thoughts are going to be eating. The male’s first thoughts are going to be mating, because that’s what he’s here for.’

The prize for creepiest anti-cannibalism stratagem goes to the wasp spider, Argiope bruennichi, so named because of its familiar yellow-and-black striped body. The most successful males seek out an underage female and then guard her until she’s on the cusp of sexual maturity.