Bitch: On the Female of the Species

by Lucy Cooke

Sperm are small and bountiful, whereas eggs are large and limited; so males will be promiscuous and females will be choosy and chaste. ‘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.

‘In the most distinct classes of the animal kingdom, with mammals, birds, reptiles, fishes, insects, and even crustaceans, the differences between the sexes follow almost exactly the same rules; the males are almost always the wooers.’ Darwin’s theory of sexual selection, outlined in The Descent of Man,

‘True women’ were expected to be pious, submissive and interested only in domesticity. They lacked passion and were not interested in sex, even after marriage. Procreation was a marital duty to be performed as part of the sacred oath, but with no relish or enthusiasm. Darwin’s theory of sexual selection chimed with these ideas. But it was perilously controversial nevertheless, far more so than natural selection. As we discovered in the last chapter, female choice was its Achilles heel. Giving such evolutionary agency to the fairer sex stuck in the throat of the Victorian patriarchy and made Darwin’s second theory distinctly unpalatable.

Despite the fact that Bateman had only tested Darwin’s theory on fruit flies, he felt confident that his conclusions could be extrapolated to far more complex organisms, like human beings. He proclaimed that a dichotomy in sex roles, namely ‘an indiscriminating eagerness’ in males and a ‘discriminating passivity’ in females, was the norm across the animal kingdom. ‘Even in a derived monogamous species (e.g. man) this sex difference might be expected to persist as a rule,’ Bateman concluded. These fixed sex roles, Bateman proposed, were underwritten by anisogamy. A female’s reproductive success is constrained by her finite number of large, energetically expensive eggs, whereas for males, a limitless supply of cheap sperm means their reproductive output is only curbed by the number of females they can win over and mate.

The trouble with this universal law is it’s not universally true.

The baffled scientists were forced to publish that male sterilization is an unsuitable means of controlling blackbird populations, citing a suspicion that ‘female promiscuity’ may be to blame. Their sheepish admission represented a fail for pest control but it foretold a revolution in our

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.

‘Because Darwin said females were monogamous, that’s what everyone believed for a hundred years,’ he said. ‘Even when there were cases that were blatantly non-monogamous, people would say they’d made a mistake or make an excuse like the female had a hormone imbalance. It was swept under the carpet.’ We now know that 90 per cent of all female birds routinely copulate with multiple males

At a meeting of the American Ornithological Society a well-known male ethology professor voiced his scepticism by telling Gowaty that the bluebirds in her study must have been ‘raped’. This, she explained to me, is physically impossible. Male songbirds have no penis.

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.

‘We even had one reviewer say that “we were kind of dumb” – the only reason females are calling like that is because we (the researchers) are on their territory trying to observe them. The female birds are actually calling at us.’

‘In most bird species, it is likely that females control the success of a copulation attempt and of transfer of sperm,’

Females across the animal kingdom began wresting back control of their sexual destiny and egg paternity from the assumed dominance of males. 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. ‘Generations of reproductive biologists assumed females to be sexually monogamous but it is now clear this is wrong,’

Hrdy was the only female graduate in her class and the focus was firmly on male animals. The halls were heavy with testosterone. ‘Sexism was built into the sciences at Harvard back then,’ she told me. The textbooks of the time considered female primates only as mothers, fundamentally nurturing and with zero competitive edge. Female primates were ‘invariably subordinate to all the adult males’ and sexual behaviour was understood to play ‘a small part in the life of an adult female’. As such they were ‘relatively identical’ and considered scientifically dull.

In dozens of female primates, such gadfly madness provokes a frenzy of sexual activity that far exceeds what’s required to fertilize the egg on offer. Some have even been observed seeking out sex when there is no egg to fertilize. Hrdy documented her langurs seducing alien males from outside the troop during pregnancy. Whilst others, such as orangutans and marmosets, show continuous receptivity and, like humans, are sexually active throughout their cycle. Such excessive behaviour is not without risks. Retaliatory attacks by possessive males, venereal disease, increased predation risks from leaving the troop, not to mention all the energy required to power this ‘excessive’ sexual activity make female philandering anything but cost-free. 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

It may come as a surprise, but all female mammals have a clitoris.

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. The shameless pleasure-seeking of many female primates would indicate otherwise. For a start, most female primates have been documented masturbating

Burton tentatively concluded that rhesus females do indeed have the ability to climax. But she noted that 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. To evolutionary psychologists like 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. According to Symons females didn’t actually evolve their own orgasms.Any

While studying her langurs in India, Hrdy observed males from outside the group routinely killing unweaned infants, as part of a troop takeover. This infanticidal behaviour, she realized, is a toxic side effect of sexual selection and male competition for mates. 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.

Perhaps unsurprisingly, a theory that sees murderous baby-eating males outsmarted by maternally driven sexual hedonism was considered somewhat heretical at first.Hrdy’s 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

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.

There are a host of other likely benefits to female philandering that include a quest for superior genes or a greater chance of genetic or immune system compatibility that then increases the survivorship of offspring.

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

How female sexuality has been transformed in the intervening 4–5 million years is open to speculation. Humans are a socially monogamous species today, but then so is the superb fairy wren. Evolutionary biologists like David M.Buss may relish the idea that all women are ultimately seeking monogamy in order to provide the best support for their kids, but if women were so naturally inclined towards fidelity then why, wonders Hrdy, is their sexuality so culturally controlled? Whether the restraining tool is slanderous language, divorce or, worse, genital mutilation there is a near universal suspicion that women will engage in promiscuous sex if left unchecked. 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

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.

If sperm are so cheap then why the seasonal adjustment? After all, as Dawkins said, ‘The word excess has no meaning for a male.’ ‘History has not been kind to this pronouncement,’ Zuleyma Tang-Martínez, emeritus professor of biology at the University of Missouri, has wryly noted. The other side of the Bateman equation – that males are preternaturally ‘eager for any female’ and their ‘fertility is seldom likely to be limited by sperm production’ – has also come under critical fire. A number of scientists have pointed out that the cost of a single spermatozoon may be trivial in comparison to an egg, but so far science has failed to discover a male that delivers just one swimming wonder at a time. Each ejaculate contains millions of sperm along with a cocktail of critical bioactive compounds, the inevitable expense of which racks up the overall biological bill4 such that in mammals, for sure, we now know that the combined energetics of a single ejaculate is in fact greater than that of an egg. As such, 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. Some, like the spiny lobster or bucktooth parrotfish, deal with this depletion issue in a Scrooge-like manner by budgeting the size of their ejaculate according to the reproductive value of the female.

Gowaty’s laser-like scientific mind identified significant issues that pointed to a bad case of confirmation bias. Bateman’s methods ‘had flaws, variances, statistical pseudo-replication, and selective presentation of data’. Gowaty concluded that ‘Bateman’s results are unreliable, his conclusions are questionable, and his observed variances are similar to those expected under random mating.’

‘It is not unheard of for some journal reviewers and editors to rebuff papers that report increased female reproductive success as a function of number of mates because “Bateman showed in 1948 that such results are not possible”.’

At the University of Oxford today, where Bateman’s paradigm is still taught, Gowaty’s critical studies don’t make the reading list, as they are considered to be ‘very political perspectives’. ‘Empirically minded biologists hear that dreaded F-word and assume it must mean “ideologically driven”,’ Sarah Blaffer Hrdy said to me. ‘What they overlooked of course was how masculinist many of their own assumptions were, how androcentric the theoretical foundations of their own Darwinian world view was.’

Then there’s monandry in which the female has just one mate, but as you’ll discover this term doesn’t need to get used that much.

The female is Goliath to his David: around 125 times his mass, and armed with giant fangs that deliver a potent venom. To seduce her, the male must gingerly traverse her enormous web – a succession of tripwires designed to sense the slightest vibration – then clamber on board her gargantuan body and copulate, all without triggering her hairpin attacking instinct. His chances of running this sexual gauntlet with life and limb intact are slim at best.For the male golden orb weaver spider sexual disappointment takes the form of a grisly death, his would-be lover literally sucking the life out of him in a matter of minutes, before hurling his desiccated carcass on to the burgeoning heap of failed suitors below.

The most famous is probably the praying mantis, a femme fatale who devours her lover’s decapitated head, while his truncated body continues to valiantly thrust away behind.

‘I remember a mating with a redknee bird-eater [Brachypelma hamorii] where we only had the one female and one male. Just as he was getting into position, she stuck her fang right through the top of his body. That was it, she literally pinned him to the ground with a centimetre-long fang and there was nothing we could do about it,’ Clarke confessed.

The female redknee, for example, has been known to live for up to thirty years, whilst males are lucky to survive to ten. This introduces a certain amount of conflict to their union. Females want to spend time fattening themselves up in order to lay lots of healthy eggs, so they’re in no hurry to mate. At the start of the breeding season, or when they’re young, females are likely to have food, and not sex, on their mind. The male on the other hand only ever has one objective, and that’s to locate a female and mate as soon as possible.

The nursery web spider, Pisaurina mira, is one of around thirty arachnids known to engage in a little light bondage during sex. The male sneaks on to the female’s web and ties her up, using a pair of specially evolved extra-long legs so he can keep clear of her fangs while looping his own silk threads around her limbs. With the female restrained, the male can mate safely and at a leisurely pace, taking time to insert his pedipalps multiple times, increasing the chance of sperm transfer and fertilization. Once the job’s done, the female releases herself from her silken fetters while the male beats a hasty retreat.

‘Even in that microsecond of her grabbing him he’d managed to insert his palp and pass on sperm. And it is just incredible that could happen,’

The fen raft male may have died a grim death, but he successfully fertilized the female’s eggs nevertheless. So his life, although short, achieved its purpose. What’s more, sucking dry her lover’s body may well have nourished the female’s eggs, giving her spiderlings a better chance in life. The male’s sacrificial act benefits both the spiderlings’ mother and their (now deceased) father and could be considered an act of extreme paternal care.

Most spiders, despite having eight eyes, can’t see very well, if at all. Much of their hunting is done by detecting surface vibrations which are imperceptible to us, using specialized slit-like organs on their legs. These vibrations are often amplified by a web, which is essentially an extension of their sensory system. The peacock spider is unusual in that it has evolved acute eyesight as well, in order to stalk and pounce on its prey, namely bugs and other spiders.

In other words, a spider suitor will act like lunch to get laid.

That combination of visual and vibratory stimuli means the male is effectively stepping into the lion’s den dressed as a steak and screaming, ‘Eat me!’ It’s a sure-fire way to get noticed, but this reckless strategy needs to be followed pretty sharply with one that stops the female from acting on her predatory impulse, otherwise the courtship’s going to be very short. ‘The fact is that spiders are predators. And so one of the best ways to draw attention is to basically trigger those things that are going to make a predator turn around and look for food. But then very quickly after that you have to say, actually, I’m not a fly or a cricket,’ Elias explained.

Spiders may even be able to sense airborne vibratory signals. Like their arthropod cousins the flies, they’re covered in long filiform hairs that can pick up air movement down to one ten-billionth of a metre, roughly the width of an atom.

Female spiders are surprisingly devoted mothers. Many carry around their eggs in a special silken sack and, once hatched, they go on to fiercely protect and feed their spiderlings, sometimes with their very own body.

Redback females are, like most spiders, promiscuous. Sperm competition means that mating does not guarantee fertilization. So for a male, dying after sex may be no different to dying before sex, if the female goes on to mate again. In the case of the redback, cannibalized males receive two paternity advantages. First, it seems they copulate for longer, which leads to their fertilizing more eggs than males that survived. Second, females were more likely to reject subsequent suitors after consuming their first mate. They were well and truly sated.

it’s not just about the calories; there must be something uniquely nutritious about eating the male.

A row of Halloween pumpkins lined up outside her lab hinted at her impish sense of humour. Brennan had instructed her students to fashion them, not with faces but with an assortment of animal vaginas for other students to identify.

When she is receptive, however, the female duck opens the lumen of the vagina so her mate can get further along her reproductive tract than unwanted males. She may not be able to choose whom she mates with but she can control the paternity of her eggs, which is, of course, the ultimate goal.

The penis-free system is undeniably awkward for the male – it is all but impossible to fertilize the female without her consent. A male can mount the female but he struggles to force his sperm inside her. So she retains control over her eggs without having to run the risk of a damaging fight. It could be that this new-found female power has even led to further significant changes in the male bird’s behaviour. Many Neoaves species are socially monogamous, with males sharing the load when it comes to parental care. Perhaps the female’s expanded sexual autonomy advanced her conflict with males over parental care also. Choosing a mate that helps around the nest rather than one that doesn’t might incite males to compete with one another to provide the best care

In his pioneering book Female Control (1996), Eberhard presented the case that female genitalia – be they vaginas, cloacae or spermathecae – are far more than just inert tubes for ejaculate. They are active organs that can store, sort and reject sperm through their architecture, physiology or chemistry. Females can dump the semen of unappealing suitors, actively speed chosen sperm on a fast track to the ova, or let them languish in a tortuous maze of ducts. The way Eberhard saw it, once insemination has taken place, it is the female who sets ‘the rules of the game

The clitoris is perhaps the only organ even more understudied than the vagina. It arrived on the anatomical map in the mid-sixteenth century, having been ‘discovered’, somewhat unconventionally, by an Italian Catholic priest called Gabriele Falloppio (1523–62).5 Falloppio was a keen anatomist and unlikely authority on female reproductive anatomy. When Falloppio’s finding was shared, however, with the great physician Vesalius, the founder of modern human anatomy, it was swiftly dismissed. Vesalius proclaimed that ‘this new and useless part’ didn’t exist in ‘healthy’ women, and was only to be found in hermaphrodites

Despite complex internal drawings by the German anatomist Kobelt detailing the full extent of the organ in the mid-nineteenth century, the clitoris was characteristically difficult to find in modern anatomical textbooks until the last gasp of the twentieth century.