Bitch: On the Female of the Species

by Lucy Cooke

In addition to male competition, Darwin knew that the mechanics of sexual selection required an element of female choice. This was trickier to explain because it gave the fairer sex an uncomfortably active role in shaping the male – something which would not go down well in Victorian England and, as we shall discover in chapter two, ultimately made Darwin’s theory of sexual selection distinctly unpalatable to the scientific patriarchy

If Marzluff and Balda had had their minds open to the female birds’ aggressive behaviour and used Ockham’s razor to shave the fluff from their conjecture, they would have got close to figuring out the pinyon jay’s complex social system. The clues that females are in fact highly competitive and play an instrumental role in the jay’s hierarchy are all there in their meticulously recorded data, but they were blind to them.

survival is an unsentimental sport and animal behaviour encompasses female narratives that range from the fabulously empowered to the terrifyingly oppressed.

The female mole’s testicular tissue is full of Leydig cells that make testosterone, but not sperm. This sex steroid hormone is commonly associated with males: beefing up muscles and fuelling aggression. It does both in the female mole, giving her the evolutionary edge underground:

The female mole forces us to confront age-old assumptions about what distinguishes the sexes. For the majority of the year, on a genital, gonadal and hormonal level, the mole sow could easily be mistaken for a boar. So, how do we know she’s a female?

Graves is confident her gloomy prophecy won’t spell the end of mankind. She’s certain that the human male would simply evolve a fresh genetic trigger for his gonads. Other mammals have already done so. A spiny rat from Japan (Tokudaia osimensis) and a Transcaucasian mole vole (Ellobius lutescens) are just two species of mammal known to have completely lost their Y chromosomes, yet hung on to their testicles. Both males and females have a solitary X chromosome and sexual development is triggered by an entirely different, and as yet unidentified, master sex-determining gene

discovered the master switch for these frogs to develop testes rather than ovaries is sometimes genetic, sometimes environmental, sometimes a bit of both. It all depends on where the frogs are from.

Crews’ research estimates that 600–800 million years ago the only creatures in existence were these cloning egg-layers. Males did not arrive on the evolutionary scene until the dawn of sex, when gametes diverged in size, which Crews reckons was around 250–350 million years later.

So, in the gospel according to Crews: Eve wasn’t created out of Adam’s rib, it was the other way round.

The idea that females – from birds to fishes to frogs to moths – are able to make sensory evaluations and exercise mate preference has been scientifically proven and accepted. Numerous studies have demonstrated how females in diverse species prefer brighter colours, louder calls, stronger odours and faster dances.

What makes a lek so special for students of sexual selection is that the females will go on to raise their offspring alone. So they’re not making their mate choice based on the resource richness of a male’s territory or his potential parenting skills – they are simply after his genes.

Gail thinks that by demanding the cocks perform this gruelling dance the hens ensure that they bag themselves a high pedigree male, with grade-A genes. ‘There’s not one single system that’s involved with making somebody a world-class athlete versus someone who isn’t, right? It’s going to be your aerobic capacity, your metabolic efficiency, your immune system, your foraging ability, how well you digest food and turn it into active energy, and so on. So the sage grouse are working their butts off doing this fundamentally difficult thing that you can only do if you are in good condition.’

Controlling the female side of this complex courtship conversation has enabled Gail to observe how changes in the hen’s behaviour affect the male’s performance. ‘We see that the males are adjusting the rate of their display according to the proximity of the females. They’re actually responding and using their energy where it would matter most.Unsuccessful guys blast away at top level all the time and then when it comes to crunch they don’t have much left to put on a great show. And that’s probably a combination of social skills and their own underlying health.’

Female satin bowerbirds are less fussed about the size of their cock and more concerned about his ability to acquire blue trinkets. Males hunt high and low to scatter the floor of their bower with anything blue they can get their beaks on – from flowers to feathers to plastic bottle tops and clothes pegs. As if this weren’t surreal enough, they have even been known to paint the walls by holding a bit of bark coated in chewed up berries in their beak. Dalí would be proud.

Previous scientists had noted male animals paying attention to female signals during courtship. But Gail was the first to show that listening and responding to her cues was linked with the male’s mating success.

Male satin bowerbirds have relatively large brains, are long-lived and undergo a strange seven-year adolescence which is spent impersonating the female. Juvenile males share the same green plumage as the females and Gail thinks that learning their complex lothario skills might explain this unusually long, cross-dressing developmental period, which is spent not only practising bower-building but being actively courted by adult males. ‘Young males learn courtship from the role of the female and they’ll often do these crouching displays. They don’t “mate”, but they’ll basically do this entire courtship from the female perspective and then if the male looks like he’s getting close to mating they just fly out the front.’

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. Such wanton duplicity is apparently standard form for the lioness, whose promiscuity is famous amongst big cat researchers – a female lion is known to mate up to one hundred times a day with multiple males during oestrus.

‘Be thou like the dunnock – the male and female impeccably faithful to each other,’ proclaimed the Reverend Frederick Morris in 1853. Morris was a keen ornithologist and author of a popular Victorian book on birds that encouraged his readers to emulate the modest lifestyle of the ‘humble and homely’ dunnock, aka the common brown hedge sparrow (Prunella modularis). The good reverend was unaware that this was in fact permission for his female flock to seek out a second lover and copulate over two hundred and fifty times with both males in order to start a family. A decree which, as Nick Davies, the Cambridge zoologist who first documented the female dunnock’s liberated sex life, wryly noted, would have resulted in ‘chaos in the parish

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. Birkhead recently discovered that species displaying the greatest sexual dimorphism hide the greatest infidelity, the most extreme known case being Australia’s superb fairy wren. As the name suggests, males boast some rather splendid blue seasonal plumage and will even woo the female, a classic little brown job, with carefully plucked yellow flowers. The male’s flamboyant courtship is rewarded with cuckoldry. At dawn his partner will slip away and have sex with the neighbours. As a result, over three quarters of the chicks in their nest, diligently provisioned by her social partner, have actually been sired by different males.

A wave of supporting evidence has now seen Hrdy’s theory of paternity confusion incorporated into mainstream academic thinking. It’s not something that sits comfortably with human morality but infanticide by males is now understood to be widespread amongst our primate cousins, being strongly suspected or actually witnessed in some fifty-one species.

Gowaty points out that had Bateman pooled all his results into one graph, and analysed the data accordingly, he could have laid claim to the first ever evidence of the benefits of female promiscuity. But Bateman, and everyone after him, focused only on the results that fitted Darwin’s proposition of promiscuous males and choosy females.

Elias has discovered that the seismic songs produced by the male have around twenty elements and are as complex as any made by humans. Each spider is essentially a freestyling jazz artist riffing on a set formula to make it his own. It was an unquestionably impressive performance, but what did it all mean?

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. Given that 80 per cent of redback males will never locate a female and die virgins, sexual cannibalism is adaptive since it significantly increases the chance that their one shot at sex hits the target and delivers the desired genetic rewards.

In the majority of duck species sex ratios are skewed towards males, so females have plenty to choose from and competition amongst drakes is fierce. As a result duck sex comes in two forms: elaborately romantic or shockingly violent.

‘It was such an obvious structure, these pouches and spirals are very big,’ she told me. Like the male’s, Brennan discovered the female’s convoluted structure is also seasonal. Which explains why the only textbook description of a duck vagina described it as a boring tube – the female was dissected outside of the breeding season.

The more we investigate the female reproductive tract, the more ownership a female gains over her fertilization rights, and the more ridiculous the idea of an all-important ‘sperm race’ becomes. It turns out that mammalian sperm aren’t even capable of fulfilling their biological function without female intervention. They can’t actually fuse with the ova without a period of activation known as capacitation. This is under female control and involves chemical alterations of the sperm, probably involving uterine secretions. But guess what? We don’t know much more because it’s not really been studied.

In the dyeing poison dart frog (Dendrobates tinctorius) females never piggyback tadpoles in the wild, it is always the male. But in the lab when O’Connell removed males she found the females often (if not always) stepped up and took on the role. When she looked inside the frogs’ brains, she found this behaviour associated with the activation of a particular type of neuron in the hypothalamus that expresses a neuropeptide called galanin, regardless of their sex. ‘The circuitry facilitating parental behaviour is the same in males and females,’ O’Connell told me.

it’s not that one sex is programmed to instinctively provide care, it’s just that one does it. But both retain the brain architecture to drive the care instinct.

Infanticide is strictly pathological in humans. We are part of the 40 per cent of mammal species that have evolved alternative strategies that eliminate the need for such a blunt survival tool. Nevertheless the same urocortin neurons still exist in the hypothalamus of humans. They’re not used, but Dulac believes they have been conserved because they’ve been so important in evolutionary history. If Dulac is right about the link between these urocortin neurons and postpartum depression, she hopes that her work can help identify drugs that could act as blockers to treat such disorders. ‘If you listen to the testimony of women who’ve killed their children, they don’t know what prompted them to do it, but they had this enormous instinct to do what they did and they have no explanation for it. You can imagine that this might be very similar to what’s happening in the brain of a mouse surrounded by danger and instinctively deciding to eliminate an infant.’

Baboons travel several kilometres every day in search of small fruits and seeds to eat. When a female gives birth, there is no downtime to recover. Though exhausted from the effort, she must keep up with her troop, carrying her infant with one hand and doing her best to maintain pace while walking on her remaining three limbs.

A breastfeeding mother has to find enough calories for two, which by the time the infant is 6–8 months old is physically impossible to do while carrying her baby – their appetite being by now too large and body too cumbersome. This creates a conflict of interests between mother and baby. In order for the mother to survive, her infant must begin to walk and forage for itself, but infants prefer to continue with the free ride, so they’ll try to manipulate their mothers using ‘psychological weapons’. These take the form of truly epic tantrums – the kind that would put a two-year-old human toddler to shame. Emotional outbursts continue until the infant has become fully independent, somewhere between its first and second birthday.

low-ranking mums live life on perpetual high alert. They must watch as their offspring are confronted by dangerous group members, yet are powerless to do anything about it. As their innate warning system screams, their anxiety increases exponentially in the face of social inequality. This stress, detected in the hormones excreted in their faeces, is thought to lower their immune response and make mothers more vulnerable to disease. It can also manifest as depression and even infant abuse. Humans are not the only primates to suffer from post-natal depression.

Abortion, at every stage of pregnancy, is an unconscious adaptive strategy for many animal mothers facing unfavourable situations that place themselves, or their offspring, in peril.

The physical process of labour is stimulated by oxytocin in the bloodstream, but the stretching of the cervix and vagina during the birthing process itself triggers an almighty rush of oxytocin in the brain. The resulting delicious cocktail of natural opiates ensures the new mother is primed to bond with her newborn as soon as it enters the world. The act of suckling will bathe her brain in yet more oxytocin, so she basically becomes addicted to caring for her baby.

An orangutan mother gets no help and as a result can only afford to have a baby every seven to eight years. By contrast the interbirth interval for a human hunter-gatherer is just two to three years. Hrdy goes on to argue that this shared guardianship favoured offspring that were good at soliciting care, thereby promoting the evolution of our unique capacity for empathy, cooperation and understanding the minds of others. In Hrdy’s version of human evolution it is sharing the caring load, not hunting and warfare, that shaped the collaborative might and brainpower of the emotionally modern human.

Unlike male birdsong, research into female song is still in its infancy. But it appears that female songbirds use their vocal abilities primarily to compete with other females. They sing to defend their territories, breeding sites or mates from other females, or to lure males away from other females. This makes much more sense in hot countries like Australia, where breeding seasons are lengthy affairs and couples remain on their territory year round.

Low-ranking females breed later, ovulate less frequently and can even spontaneously abort as a result of being persistently terrorized by dominants. As Sarah Blaffer Hrdy notes, across primate species ‘high rank carries with it not only freedom from harassment and exploitation by more dominant females, but also this sinister prerogative to interfere in the reproduction of other females’. This low blow to a female’s fertility has grave consequences, arguably far greater than the most savage canine-baring contest between males. It hits a female where it really hurts, in her precious genetic legacy. Being prevented from breeding is the most ruinous punishment there is. Just because fists aren’t flying 24/7, it’s naive to assume female primates are not as competitive as males. They just fight craftier and dirtier.

In the event that a developing female meerkat’s hormones override the system, and she has the temerity to get knocked up by a roving male, retaliation is swift and terminal. The pregnant subordinate will be unceremoniously evicted. The ensuing stress generally triggers her to abort. If she manages to go full term without detection and give birth in the den, the matriarch will kill and eat any unwelcome pups – very often her own grandchildren – and banish the female from the group.

One thing you won’t see is subordinate females ganging up to overthrow the top bitch. ‘That’s what a primate would do. Have an alliance and take on the dominant,’ Clutton-Brock explained. ‘Meerkats don’t form alliances. They’re very stupid – they’re certainly not what you’d want to rely on to decide your insurance policy.’

Naked mole rats produce a novel type of hyaluronan – the same interstitial gloop you’ll find in expensive face creams promising eternal youth. It makes their skin extra-specially elastic and as an added bonus it might also be the reason they don’t get cancer.

‘99.99 per cent of the colony will never reproduce,’ Faulkes told me. Unlike meerkats, subordinates never flout the no-breeding rule with sneaky copulations. They can’t. The queen has put paid to any notion of parenthood by suppressing their sexual development. Both male and female subordinates remain trapped in a pre-pubescent state. They don’t even develop adult genitalia. So subordinate sex is ruled out in this eusocial system. As a result, Faulkes tells me, the non-breeding castes are impossible to tell apart sexually. They scuttle about the colony like unisex smoothies doing the queen’s bidding.

Faulkes believes that these antagonistic cues from the queen translate into a state of ‘stress’, which alters the subordinate’s brain chemistry and impinges on the hypothalamus, the area of the brain responsible for controlling reproduction.

For the queen to maintain her dominance throughout the colony takes some serious legwork. ‘We know she expends enormous amounts of energy patrolling the colony. We found that the queen is more than twice as active as the next most active animal in the colony and travelled three times the distance over the space of about eighteen months,’ Faulkes explained to

Colonies can function for years, if not decades, in a state of peaceful industry as long as the queen is a dominant, mobile presence. But if she is weakened or removed for any reason, all hell breaks loose. Her absence will trigger the next highest-ranking females to become sexually mature within a week and then, very rapidly, it all turns very Game of Thrones.

These professional burrowers have evolved a ferocious bite. A quarter of their entire body musculature is devoted to powering their jaws to crunch through baked earth – and then there’s those javelin teeth. When females turn these industrial excavation tools into weapons things get ugly

It’s the same story with most lemur species. This peculiar group of primates, found only on the island of Madagascar, are largely female dominant. Whether they’re in monogamous partnerships, like the eerie singing Indri (Indri indrii), or polygamous societies, like the black-and-white ruffed lemur we met earlier, in 90 per cent of the 111 species it is the females who call the shots sexually, socially and politically. Madagascar is an island of bossy bitches – a land where female primates rule.

Jolly felt that where these three evolutionary lines – the lemur, the New World monkey and the Old World monkey – converged offered valuable insights into our shared ancestor, ‘the not-quite-monkey who first formed social bonds with others of its kind’. Her discovery of this early branch of fierce, frightening females eroded the idea that aggressive male patriarchy is the natural state of affairs for all primates.

Old World monkeys make for poor primate prototypes. Their behaviour is actually highly derived, tailored to meet specific environmental challenges and far from representative.

Chimpanzees are famously territorial. When neighbouring groups meet, the scene is extremely hostile: males tear about with their hair on end, their body language set to intimidate. They scream, bang on trees and will even kill each other. In stark contrast, when bonobo groups meet there is no sign of fighting. ‘They might shout a little bit in the beginning, but very soon it looks more like a picnic than warfare,’ Frans de Waal told me. Albeit a picnic where everyone is having sex with each other.

A foraging lifestyle makes it much harder for males to restrict females’ movements and access to resources, as they are able to source their own. Once females were restricted in their activities and males gained control of high-quality foodstuffs, like meat, females lost agency and became sexual property.