Preface. This is a review of Cooke’s book “Bitch: On the female of the species”. I’ve been reading about evolution for a long time, but there was a great deal of new research on the role females play in evolution I was shocked at how little I’d read about.  This is probably because most research on evolution since Darwin has been done by men focusing on male animals.  The females of species were seen not worth bothering with. They were passive, had nothing to do with how their species evolved, being the submissive obedient sex. But now that women have entered the field, Cooke cites a great deal of interesting research on why men got it all wrong. She writes:

“In the beginning there was female, and she gave rise to male. From this alternative evolutionary perspective, the ultimate answer to what is a female is: she’s the ancestral sex. Relics of this primal egg-layer exist within all of us. Which puts a fresh spin on males getting in touch with their feminine side.

Try explaining the need to be passive to a dominant female spotted hyena, and she’ll laugh in your face, after she’s bitten it off. Female animals are just as promiscuous, competitive, aggressive, dominant and dynamic as males. They have equal right to drive the bus of change. It’s just that Darwin, along with the coterie of gentlemen zoologists that helped inform his argument, couldn’t, or perhaps wouldn’t, see them that way.

Darwin’s strict sex roles have forced an abandonment of this fundamental scientific process as researchers are compelled to dream up ever more tortuous excuses to explain away female behaviors that deviate from the standard stereotype.“

Another profound insight into human evolution I learned is that it wasn’t hunting and warfare, but more likely shared child-rearing that made us human. Darwin proposed that increasingly skilled male hunters led to the evolution of ‘greater intellectual vigor and power of invention of man’. But primatologist Sara Hrdy believes that because women helped each other raise children, this “favored offspring that were good at soliciting care, thus promoting the evolution of our unique capacity for empathy, cooperation and understanding the minds of others. It is sharing the caring load, not hunting and warfare, that shaped the collaborative might and brainpower of the emotionally modern human.”

Women researchers discovered that across many species, females were promiscuous and why. Though Hrdy wondered, since research done by men found “females were naturally inclined towards fidelity, why was the sexuality of human women 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 is that patriarchal social systems evolved in order to curb and confine it.”

Cooke added that “Back when we were all hunters and gatherers, women had a lot more freedom, because it was hard for males to restrict females’ movements and access to resources, since they could get food and resources on their own. But once females were restricted in their activities and males gained control of high-quality foodstuffs, like meat, females lost agency and became sexual property. Paternity became an issue, as property was inherited, and patriarchy took hold. The evolution of the capacity for language allowed males to consolidate and increase their control over females because it enabled the creation and propagation of ideologies of male dominance/female subordinance and male supremacy/female inferiority.

But it doesn’t have to be this way. Males are not genetically programmed to aggressively dominate females. Across species, their ability to do so depends on environmental and social factors. The key ingredient for female empowerment is the strength of the sisterhood, from family to friends, to overthrow an oppressive patriarchy and foster a more egalitarian society.

We have a lot to learn from bonobo females. The feminist movement argues that if you behave with unrelated females as if they are your sisters, you can gain power. The bonobos show us that that’s true. It gives us a lot of hope.”

Below are my kindle notes — but you really ought to read all of this funny, insightful, and brilliant book, I’ve left so much out below and selected material I might want to draw on for future posts.

Women’s evolution in the news:

Alex B (2023) Worldwide survey kills the myth of ‘Man the Hunter’. Women hunt in vast majority of foraging societies, upending old stereotypes. Science

See the full scientific paper here at Plos One

Research of 1400 anthropological reports from the past century revealed  that women hunted in nearly 80% of surveyed forager societies, smashing the long-standing myth that men hunt, women gather, and that this division runs deep in human history. For decades anthropologists have witnessed forager women—those who live in societies that both hunt and gather—around the world skillfully slay prey: In the 1980s, Agta women of the Philippines drew bows and arrows as tall as themselves and aimed at wild pigs and deer, and Matses Amazonians struck paca rodents with machetes. Observations from the 1990s described Aka great-grandmothers and girls as young as age 5 trapping duiker and porcupine in central Africa. A study published today in PLOS ONE has united these reports for a first-of-its-kind global view of women hunters. Reviewing accounts penned by scholars who study culture, known as ethnographers, as well as those by observers between the late 1800s and today.

Alice Friedemann  www.energyskeptic.com  Author of Life After Fossil Fuels: A Reality Check on Alternative Energy; When Trucks Stop Running: Energy and the Future of Transportation”, Barriers to Making Algal Biofuels, & “Crunch! Whole Grain Artisan Chips and Crackers”.  Women in ecology  Podcasts: WGBH, Jore, Planet: Critical, Crazy Town, Collapse Chronicles, Derrick Jensen, Practical Prepping, Kunstler 253 &278, Peak Prosperity,  Index of best energyskeptic posts

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Cooke L (2022) Bitch: On the Female of the Species

A sexist mythology has been baked into biology, and it distorts the way we perceive female animals. In the natural world female form and role varies wildly to encompass a fascinating spectrum of anatomies and behaviors. Yes, the doting mother is among them, but so is the jacana bird that abandons her eggs and leaves them to a harem of cuckolded males to raise. Females can be faithful, but only 7% of species are sexually monogamous, which leaves a lot of philandering females seeking sex with multiple partners. Not all animal societies are dominated by males by any means; alpha females have evolved across a variety of classes and their authority ranges from benevolent (bonobos) to brutal (bees).

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, which ultimately made Darwin’s theory of sexual selection distinctly unpalatable to the scientific patriarchy

Darwin’s branding of the sexes as active (male) and passive (female) could not have been more effective if it had been devised by a multi-million-dollar marketing company with an unlimited budget. Darwin was probably not the originator of this convenient sexual classification. He likely borrowed it from Aristotle, the father of zoology. In Aristotle’s partitioning of the sex roles. ‘In those animals that have… two sexes… the male stands for effective and active… and the female… for the passive.’

The main problem with this neat binary classification is: it’s wrong.  There is little doubt that the first creatures reproduced by cloning.

The earliest reproductive organism had to be able to lay eggs and that’s a female, so about 600–800 million years ago the only creatures in existence were cloning egg-layers. Males did not arrive on the evolutionary scene until the dawn of sex, when gametes diverged in size, around 250–350 million years later. With this divergence came the need for complementary behaviors to facilitate the union of these different-sized gametes; individuals must locate one another, become sexually attracted and reproduce. So sexual dimorphisms evolved that were activated by androgens. Maleness evolved as an adaptation to femaleness. When males came along what they did was to facilitate reproduction in the female. To stimulate and coordinate the neuroendocrinological processes that underlie the shedding of gametes. Males are behavioral facilitators. If males are the derived sex, that evolved out of the original female, it is logical to assume they must contain evolutionary traces of egg-makers. And, it turns out, they do.

Oestrogen has to be the original steroid hormone because the ancestral animals only produced eggs, and eggs produce oestrogen. The oestrogen receptor is important in virtually every tissue of the body, there is no tissue in the body that doesn’t have an oestrogen receptor.  The “female” sex steroid has a critical role even in males, because males were originally females. So Eve wasn’t created out of Adam’s rib, it was the other way round.

In the beginning there was female, and she gave rise to male. From this alternative evolutionary perspective, the ultimate answer to what is a female is: she’s the ancestral sex. Relics of this primal egg-layer exist within all of us. Which puts a fresh spin on males getting in touch with their feminine side.

Try explaining the need to be passive to a dominant female spotted hyena, and she’ll laugh in your face, after she’s bitten it off. Female animals are just as promiscuous, competitive, aggressive, dominant and dynamic as males. They have equal right to drive the bus of change. It’s just that Darwin, along with the coterie of gentlemen zoologists that helped inform his argument, couldn’t, or perhaps wouldn’t, see them that way.

Darwin’s strict sex roles have forced an abandonment of this fundamental scientific process as researchers are compelled to dream up ever more tortuous excuses to explain away female behaviors that deviate from the standard stereotype.

Take the pinyon jay. Highly intelligent creatures with such active social lives are likely to have some means of ordering their busy society – a dominance network – otherwise there would be chaos. So they went in search of the ‘alpha male’. But the jays refused to engage in battle. The researchers were forced to base their scale of combat on some fairly subtle cues, like sideways glances.

The curious thing is, the researchers had seen jays behaving with significantly more antagonism than a few annoyed looks. They documented birds in dramatic airborne battles where dueling pairs became locked in combat mid-air and ‘flap vigorously as they fall to the ground’ where they ‘peck at each other with forceful stabs’. These encounters were ‘the most aggressive behavior observed during the year’, but they were not included in any dominance network as the perpetrators weren’t male. They were all female. The authors concluded that this ‘testy’ feminine behavior must be hormonally driven. They proposed that a spring hormone surge had given these female jays ‘the avian equivalent of PMS which we call PBS (pre-breeding syndrome)’! There is no such thing as avian PBS. If Marzluff and Balda had had their minds open to the female birds’ aggressive behavior 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.

It hasn’t helped that the academic establishment was, and in many areas still is, dominated by men who naturally view the animal kingdom from their standpoint; the questions asked to inspire research thus originated from a male perspective. Many simply weren’t curious about females. Males were the main event and became the model organism – the default from which the female deviated, the standard by which the species was judged.

The most dangerous thing about sexist bias is its boomerang nature. What started as chauvinist Victorian culture was incubated by a century of science and then spat back into society as political weaponry, rubber-stamped by Darwin. It gave a handful of, notably male, devotees of the new science of evolutionary psychology the ideological authority to claim that a host of grim male behaviors – from rape to compulsive skirt chasing to male supremacy – were ‘only natural’ for humans, because Darwin said so. They told women they had dysfunctional orgasms, that they could never break through the glass ceiling thanks to an innate lack of ambition, and should stick to mothering.

The second wave of feminism opened once-closed laboratory doors and women were walking the halls of top universities and studying Darwin for themselves. They were heading into the field and observing female animals with the same curiosity as male animals. They discovered sexually precocious female monkeys and, instead of ignoring them like their male predecessors had, they questioned why they might be behaving in this way. They developed standardized techniques for measuring behavior that forced equal attention on both sexes. They harnessed new technologies to spy on female birds and reveal that far from being victims of male sexual dominance, they were in fact running the show.

The female mole is indeed a wondrous creature. A solo operator who makes her living by hunting worms using a network of tunnels that act as her own form of animal trap. When a worm pushes through her subway ceiling, she quickly sniffs it out using a long pink snout that can actually smell in stereo – each nostril acts independently, allowing her brain to accurately compute the direction of dinner in the pitch black. Her quarry, once caught, isn’t killed immediately; instead, the mole paralyses it with her venomous saliva so it can be stored alive in a specially constructed larder without turning to rot. As many as 470 wrigglers have been recorded in one lucky mole’s pantry, which is helpful as she needs to consume over half her body weight in worms a day. Life underground is tough. Burrowing earth is exhausting work and there’s comparatively little oxygen to breathe. To survive this hostile environment evolution has equipped the mole with some cunning specializations. Her blood sports a modified form of hemoglobin that increases her affinity for oxygen and tolerance of toxic waste gases.

But perhaps most impressive of all are the female mole’s balls. The mole sow’s gonads are described as ‘ovotestes’. These internal reproductive organs consist of ovarian tissue at one end and testicular tissue at the other. The ovary side produces eggs and expands during the short breeding season. But, once the job of reproduction is done, this egg-making tissue shrinks and the testicular tissue expands until it is actually larger than the ovarian. 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 fueling aggression. It does both in the female mole, giving her the evolutionary edge underground: extra digging power and added hostility for defending her pups and worm larder.

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?

Many would consider genitals an easy indicator of sex. But the female mole’s ‘phallus’ blows that notion clean out of the water. She’s no freak. Dozens of female animals from tiny cave-dwelling barklice to giant African elephants, sport ambiguous sexual anatomy that’s commonly described in phallic terms.

There’s no such thing as a “male” hormone or a “female” hormone. It’s a common misconception. We all have the same hormones. All that differs between males and females are the relative amounts of enzymes that convert the sex steroids from one to another and the distribution and sensitivity of hormone receptors.

The idea that any development process could be ‘passive’ is clearly quite ludicrous – ovaries require just as much active assembly as do testes. Yet for 50 years the ‘default’ female system went unstudied. Sexual differentiation isn’t about describing how you get females and males. It’s only about describing how you get males. For decades people were happy not to have an explanation of how you get the female form and just saying, “Well, it’s passive.”

Things are improving. The unknown land of ovarian development has now been partially explored, but its genetic map is far emptier than the one that exists for testes. The way sex is taught, you’d be forgiven for assuming the genes for creating testes inhabit the Y and the genes for ovaries reside on the X. It’s much more complicated than that. The entire process of sex organ determination involves an orchestra of around 60 genes working in concert. These sex-determining genes don’t all exist on the sex chromosomes, let alone sit in a disciplined and gendered fashion on either the X or the Y. They are, in reality, scattered haphazardly throughout the genome. SRY is like their conductor. If this crucial testes-determining trigger is present it instructs these sex-determining genes to start playing in the key of T for testes. If SRY is absent they’ll play in the key of O for ovary.

This is where sex becomes fabulously complicated. Aside from SRY, this orchestra of 0sex-determining genes is basically the same in males and females. These genes have the ability to create either ovaries or testes, but exactly which gonad they actually produce depends on a complex network of inter-gene negotiation. And these sixty or so genes are remarkably conserved across all vertebrates. Birds, reptiles, amphibians and fish all have more or less the same set of genes as mammals for creating a testis or an ovary. What differs, however, is the master switch that kicks off the pathways.

Heat is just one of several known external sex-determination stimuli. Exposure to sunlight, parasitic infections, pH levels, salinity, water quality, nutrition, oxygen pressure, population density and social circumstance – how many of the opposite sex are in your neighborhood – can all influence an animal’s sexual fate. In some animals sex determination can be controlled by any, or indeed many, of the above. Which means sex can get very confusing indeed if, for example, you are a frog.

Female Choice

Darwin proposed that sexual selection could be responsible for the exceptional evolution of human cognition – especially the more ‘self-expressive’ aspects of human behavior, such as art, morality, language and creativity. The idea that female choice might have polished the human brain into brilliance would have been the ultimate blow to the Victorian scientific patriarchy – hitting them right between the eyes, where it hurt most.

Darwin’s controversial claim that females were not only sexually autonomous but had the wherewithal to make decisions shaping male evolution put the fairer sex in a very powerful role – a role that made most (male) biologists deeply uncomfortable. Men controlled women in Victorian England – not the other way around. This Victorian establishment was not pleased. Beauty was God-given, so the idea that female sexual preference was the primary agent of its evolution was tantamount to heresy.

His most influential detractor was Alfred Wallace, who saw no need for a bogus new evolutionary theory to explain male courtship ornaments and display, which he believed were simply a result of the male’s ‘surplus of strength, vitality, and growth-power’.  His trashing of female choice meant that Darwin’s second great theory of sexual selection became ‘the mad aunt in the evolutionary attic of Darwinian theory’, which, apart from a couple of exceptions, wasn’t allowed out to play for one hundred years.

Few animal courtships are as strange or, quite frankly, as silly as that of the greater sage grouse. The overall effect of the male dancing is pure Monty Python and begs the question, Evolution, what were you thinking? What perverse force could have shaped such preposterousness? The answer: female choice. Female animals have rather a lot to answer for. Why does the male proboscis monkey have such a long and pendulous nose? Well, the ladies apparently like it that way.

The sexual revolution of the 1970s and the impact of feminism on evolutionary biology have helped stir Darwin’s daring idea from its century-long slumber. 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.

Leks are the most extreme seduction marketplace – a winner-takes-all situation where a lucky few bachelors will dominate the mating scene: 70–80% of copulations on leks – from insects to mammals – are attributed to only 10–20% of the males.  During the peak of mating the sage grouse lek is a madhouse.  Most of the mating happens in just three days, with the females often in one big scrum, fighting with each other for their position around the top cock.

The sage grouse’s beatboxing strut looks as strenuous as it is bizarre. How much energy it costs the cocks is hard to say, but a recent study on great snipe, another lekking species, that courts females by drumming its wings, found they lose almost 7% of their body mass after every daily courtship session. So there are likely some serious energetic costs for the male sage grouse, especially since their sagebrush is so low in energy. On top of that the leaves are also highly toxic, so the males are essentially dancing their guts out while coping with the avian equivalent of a massive hangover.

By demanding the cocks to perform this grueling dance the hens ensure that they bag themselves a high pedigree male, with grade-A genes aerobic capacity, metabolic efficiency, immune system, foraging ability, how well you digest food and turn it into active energy, and so on.

The acoustics of the males’ beatboxing had a weird four-pronged pattern of sound radiation that means their calls are actually quietest directly in front of the displaying bird and loudest to the sides and behind. So although the strutting male appears to be turning his back on a female, he is actually blasting his rubbery plops directly at her. Top cocks are not simply the loudest dancers on the lek, they also need to respond to subtle cues given by the females. Meaning they need to listen as well as they can dance.

The female is playing a much more active role – either eliciting the male display she wants or shaping the male displays – and he has to respond in order to be attractive and not just be flashy.

Previous scientists had noted male animals paying attention to female signals during courtship. Sage grouse researchers were the first to show that listening and responding to her cues was linked with the male’s mating success. Not only that, but in the case of the bowerbird, these social skills are equally as important as the intensity of his display for the male to be successful.

Female sage grouse may also be paying attention to each other. Young female guppies are known to emulate older (and perhaps wiser) female fishes’ mate choice decisions. Such ‘eavesdropping’ may also contribute to the insane allure of dominant male sage grouse. If 80 females are around a male then it’s hard to imagine they all made an independent decision.

Social intelligence

Sexual selection can drive the evolution of these flashy traits, but also this kind of social intelligence, these courtship tactics that are also an important part of competition for mates. So sexual selection might be a lot more powerful than we initially assumed. All this tactical negotiation requires cognitive power. 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 learning their complex lothario skills might explain this unusually long, cross-dressing developmental period, which is spent not only practicing 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.

A study in 2009 that tested the male satin bowerbirds’ problem-solving skills was the first to show that cognitive performance is associated with mating success and females prefer the most nimble-minded male. Male budgerigars that demonstrate their problem-solving smarts have also been shown to be more attractive to females. So female choice could be responsible for shaping not only a male’s body and behavior but also his brain.

Promiscuity among females – why?

Darwin’s theory of sexual selection, outlined in The Descent of Man, continues in the vein of a Mills & Boon romantic novel by stating that male animals have ‘stronger passions’ and fight amongst themselves to ‘sedulously display their charms before the female’. The female, on the other hand, ‘with the rarest of exceptions, is less eager than the male. She generally “requires to be courted”; she is coy.’ Her job is to passively yield to the winning male’s charms, or choose among the ‘wooers’ and concede to their sexual demands, albeit reluctantly. Darwin noted that the female’s demure nature is such that ‘she may often be seen endeavoring for a long time to escape from the male’.

‘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.

Trivers argued that whichever sex invests least in offspring will compete to mate with the sex that invests the most.

Other (male) scientists even justify the worst human male behavior – 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.

On a safari, the roars of a male lion were played over a speaker.  This attracted not just one, but three large lions, two males and a female, who padded around the vehicle, looking for a male lion. When they found nothing, the two males wandered off, but the female lay down in front of our vehicle, pinning us to the spot for over an hour. She was likely in estrus and consorting with one of the two makes, but had chosen to abandon her mate and remain by the source of our roar because she was hoping to cop some extra-curricular sex with its owner. 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 100 times a day with multiple males during estrus.

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. How could one sex be promiscuous and the other chaste – after all, who were the males having sex with if the females were all so demure?

We now know that 90% 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.  And species with the greatest sexual dimorphism have the greatest infidelity. Female birds are sneaky about their extra-pair affairs. Their duplicity was only found using forensic DNA.

The first person to utilize this novel technology to investigate female songbird fidelity was Patricia Gowaty. It was also her first taste of being ignored by the male scientific establishment. ‘I got a lot of flak from this study,’ she told me over the phone in a disarming southern drawl. ‘It was terrible, Lucy. It was as though I’d discovered something, but it offended so many people that it was unbelievable.’

Gowaty’s subject was the eastern bluebird, the cobalt-colored 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.

At a meeting of the American Ornithological Society a well-known male ethology professor voiced his skepticism 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. Both sexes have a multi-purpose hole called a cloaca that is used to transfer gametes and waste. In order for fertilization to happen both male and female must evert the middle section of their cloaca so that they touch in what biologists call a ‘cloacal kiss’. This must be done while the male is balancing precariously on the female’s back, so the female can call a halt to any unwelcome sexual shenanigans simply by flying off.

The ensuing decade saw a flurry of bird paternity studies and a tidal wave of evidence that could no longer be ignored. Yet somehow female birds remained resolutely coy in the eyes of the (male) ornithological establishment. After all, the law according to Darwin-Bateman-Trivers stated that females had nothing to gain from multiple matings, and everything to lose – if her social partner were to catch her, it was believed an adulterous female would run the risk of being deserted or, worse, killed.

Over the course of 14 breeding seasons she noted that 70% of female dalliances took place shortly after dawn in the territory of a male higher-ranking than the bird’s social partner. It looked suspiciously like female birds shacked up with Mr Average were sneaking off to their neighbor, Mr Fabulous, for some superior genes. Stutchbury discovered that females aren’t victims at all, but actively advertising their fertility with a special chip chip call that lets neighboring males know a female’s up for some extra-pair sex.

Female hooded warblers would also leave their territory to scope out the local talent, but only during their fertile period. This they did by listening to the male warblers’ warbling. Females paired with meek males that didn’t sing that much would leave their home territory the most and seek out sex with a more strident stud.

Here was trustworthy 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.

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% of known species.

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 behavior was understood to play ‘a small part in the life of an adult female’. As such they were ‘relatively identical’ and considered scientifically dull. There was much weeding to be done.

A wild chimpanzee female will produce only five or so young in a lifetime yet she will avidly engage in some 6,000 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. Barbary macaque females are equally lustful, with one female recorded having sex at least once every 17 minutes with every sexually mature male in the group (of 11). Savannah baboons have been documented badgering males for sex with such frequency during their estrus that their lustful advances are even refused. 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.

Such excessive behavior 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 has said.  What’s more, many females appear to be rather enjoying it. 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 – both in zoos and in the wild.

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 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 clitoral morphology screams adaptation. ‘I cannot understand why these old canards persist.’ Comparative anatomical studies are thin on the ground but in promiscuous multi-male breeders – like baboons and chimps – the clitoris is especially well developed, reaching an inch or more in length. It is also positioned at the base of the vagina, where it can receive direct stimulation during sex. Which suggests that these females are being rewarded with significant pleasure for the sex they have with multiple partners. But why?

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 behavior, she realized, is a toxic side effect of sexual selection and male competition for mates. Rather than his having to wait 2-3 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 estrus, making her readily available for fertilization. As a defense 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. Hrdy’s theory explains why that first female langur she saw was heading off from her group to solicit a band of foreign males and why others were seen having sex with alien males during pregnancy. Far from being ‘wanton’, their overt sexual behavior is in Hrdy’s eyes ‘assiduously maternal’ – evolution’s cunning ploy to increase the survivorship of their young.

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

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 51 species. In almost all cases, males only attack when entering the breeding system from outside it, specifically targeting unweaned infants.

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. 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.

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. DNA fingerprinting has revealed that dunnock males were often, but not always, accurate in their paternity ‘assessments’

Hrdy revealed that all across the primate world males are manipulated into caring for babies that may or may not be theirs. This unequivocal fact pours cold water on the common theory that monogamy is a female’s best strategy because males will only care for young they know are theirs. ‘Non-conceptive sexual behavior, while not increasing fertilizations, increases infant survivorship, and as such is the ultimate female reproductive strategy,’ Hrdy says. She’s certain this polyamorous maternal tactic could have been especially useful for our human ancestors in helping them raise an exceptionally slow-maturing infant, which demands years of care before reaching independence.

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.

Sperm Competition

It all comes down to sperm competition. Large testicles produce sperm at a higher rate, giving the male a better chance of either filling a female’s reproductive tracts so that no further sperm can be deposited, or swamping out the male that got there first. 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. Human testicles, you will be keen to know, fall somewhere in the middle of these two

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.

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 bill 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, perhaps why Drosophila melanogaster semen is spiked with anti-aphrodisiacs that warp female behavior, making her wait longer before mating again; a chemical chastity belt that induces a certain coyness.

Gowaty points out that had male researchers could have pooled their results into one graph, and analyzed the data accordingly to discover the benefits of female promiscuity. But they all focused only on the results that fitted Darwin’s proposition of promiscuous males and choosy females.

Why do females eat their mates?

The female spider’s penchant for rolling dinner and date into one was an affront to male Victorian zoologists on several counts. Here was a female that deviated from the passive, coy and monogamous template by being vicious, promiscuous and unquestionably dominant. She also represented something of an evolutionary conundrum. If the point of life is to pass on your genes to the next generation, then eating your potential sexual partner instead of mating with him seems maladaptive. Yet sexual cannibalism is common amongst spiders of all kinds, along with a host of other invertebrates, from scorpions to nudibranchs to octopus.

I had no idea that the big spiders in the middle of the webs are always female. Male spiders are generally weedy itinerant creatures with little time for web-building or indeed hunting, and their fangs and venom sacs are often puny in comparison. The female spider is the one to sport the more toxic venom and construct the most elaborate webs.

Some of the most dramatic sexual liaisons are between the bird-eating spiders. These are the titans of the spider world, with legs that can span up to 30 centimeters. Position is everything with spider sex, and every species has its preferred angle from the spider sutra. Most bird-eaters favor face to face, although one bold Brazilian species will flip a female back into missionary position for easy access. The male must reach underneath the female’s abdomen to insert his pedipalps into the female’s twin genital slits, one at a time. In the case of the bird-eating spiders, all this must be negotiated whilst holding on to the female’s fangs.

Spider breeders need to be  on standby with a pot or ruler to intervene if things start to get ugly. Damaged suitors can be rescued and reused, even with lost limbs, especially if they are in short supply. But once the fang is in, venom and digestive enzymes are swiftly injected and the male’s organs melt into a spider Slurpee, ready to be sucked up by the female. The most crucial trick to stop a female from eating the male is to ensure the female has been wined and dined before introducing the eight-legged Casanova, because if she hasn’t eaten for a while her first thoughts are going to be eating.

Reproduction may be the point of life, but male and female spiders are working to different timeframes. Females are not just bigger, they also tend to live several times longer than the males. The female redknee can live up to 30 years, whilst males are lucky to survive to 10. 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. Which puts females in charge, since they live much longer.

Love is a battlefield and sexual conflict is now understood to be a major evolutionary force that works antagonistically between the sexes. The tug of war of opposing interests provokes an evolutionary arms race of adaptations and counter-adaptations as each sex tries to outfox the other and get what they want. At the most basic level, many orb weaver males have learned to wait patiently at the edge of the female’s web until their paramour is consuming her lunch, possibly one of their love rivals, before making their move. Others, like the male black widow, can actually smell if their fancy is hungry from the sex pheromones on her silk, and keep a wide berth if she is. Then there are those that arrive on their date lugging dead things wrapped in silk – the spider equivalent of a box of fancy chocolates – to occupy the female’s jaws while the male gets down to business with his palps.

The nursery web spider is one of around 30 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.

When danger threatens, the male nephilid orb weaver spider snaps off his pedipalp and makes good his escape, leaving the palp to pump sperm without him. As an added bonus, his mutilated genital plugs the female’s epigynum, preventing her mating with another male. The downside, however, is that the self-inflicted eunuchs are themselves functionally sterile – a one-hit wonder.

Spider breeding isn’t easy. You’ve got the music on and the lights turned down low, and the female is just not moving. She’s paying no attention whatsoever. That is really frustrating, and that happens a lot. In the wild males may have to travel treacherously long distances, avoiding a host of hungry predators and fighting off other males, in order to locate a female. They may only have one shot at sex, so getting noticed is key, even if it results in death.

Captive breeding doesn’t get much more pressurized than when it involves an endangered species, let alone a cannibalistic spider.  One breeder had to deal with an audience of anxious conservationists scrutinizing his technique as well as the future of the species resting on his shoulders.  He’d done his best to replicate the spider’s wetland home with a large tank complete with mini water-weed islands, just like the spiders like it. As well as ensuring that the female was well-nourished and making sure the couple had plenty of space. Fen raft spiders have a protracted courtship in the wild, involving the male following the female around for some time, so the female had plenty of room to maneuver and not get trapped in a corner and freak out, which can also trigger an attack. Things were going ‘swimmingly’. The male had made a number of tentative approaches by bobbing his body and vibrating his legs in delicate arcs on the water around her. The female appeared tranquil and receptive as the male moved in closer. Once within reach, tactile caresses are understood to pacify an aggressive female and form a key part of a male spider’s seduction routine. The fen raft suitor began to vibrate his legs across the female’s body and cautiously maneuver himself into the correct position to insert his pedipalps. Then, in a split second, she grabbed him and killed him. The assembled audience could only look on in horror as the female spider greedily demolished what could have been the savior of her species.

A month or so later, he was surprised to find a large silken cup in her enclosure. It was an egg sac. It seems male fen raft spiders can be fiendishly quick on the draw with their sperm pistol pedipalps, even when getting munched.

When approaching a female in the scrub of his native Australia, a fuzzy little four-millimeter spider stages an unexpectedly elaborate dance routine by abruptly lifting his furry abdomen into a vertical position and unfurling two shimmering flaps decorated with graphic blues, oranges and reds that could have been designed by Gianni Versace. This peacock arachnid waggles his gaudy butt-fan, whilst bobbing his body up and down, stomping his feet and waving a pair of oversized legs in the air. This exuberant routine, part Fred Astaire and part Village People, can go on for up to an hour until he’s close enough to make his move. It is an undeniably charming spectacle, made all the more endearing by the fact that the peacock male is, of course, dancing for his life. Up to three quarters of peacock suitors are terminally dispatched by an unimpressed female.

‘I love them with all my heart,’ Damian Elias, associate professor at University of California, Berkeley, told me from behind a pair of thick-framed glasses and a mop of unruly hair. I had already guessed his feelings by the plethora of toy spider kitsch decorating his lab alongside posters of indie rock bands I’d never heard of. Elias has been studying spider seduction for almost two decades and has combined his twin passions – spiders and music – by discovering that the peacock male isn’t just dancing, he’s dropping major beats too. The seismic songs produced by the male have around 20 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.

Arachnids inhabit a very different sensory world to us. Most spiders, despite having 8 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.

The peacock spider’s two outsized marble-like eyes have both a telephoto lens and color vision – an extraordinary evolutionary achievement for an ancient invertebrate – so they’re well suited to detect the male’s outlandish fan dance. But Elias has discovered the female peacock spider is also using a seismic sense that’s imperceptible to us.  The peacock spider’s flamboyant routine is the ultimate dance with death. Its extravagant nature is designed to show off the male’s vigor, but also to grab the attention of a female who may be busy hunting (things that look like him) and not exactly thinking about sex. Creatures with small brains, like spiders, have a limited sensory world, so punching through the environmental noise to get noticed isn’t easy, so a spider suitor will act like lunch to get laid.

Female jumping spiders have their predatory instinct triggered by flickering motions made by prey in their peripheral vision, detected using their smaller eyes. This could be why the male peacock starts his seduction routine with jazz hands as this imitates the jerky movements of a tasty insect. Vibrations are probably also important, especially for other less-visual spiders. Many males start their seduction routine with tremors that mimic a struggling insect in a web. These spark the female’s hunting instinct from a distance, before she even sees or smells him. But then very quickly after that you have to say, actually, I’m not a fly or a cricket.’  This energetic display also indicates the health and vigor of a suitor, enabling the female to decide which males get lucky and which get chomped. Females like big males and it’s thought that a male’s size is betrayed by his vibrations. All that fan waving and butt shimmying may also serve another function: to hypnotize the female into quiescence.

Digging into the peacock female’s discernment, Elias found they became aggressive when males made less vibratory effort, failed to coordinate their song and dance routine or, worse still, if they didn’t pay attention to her signals.

Darwin assumed the exceptional size difference in spiders to be a result of sexual selection acting on the male: a dwarf can more easily escape the ‘ferocity of the female by gliding about and playing hide and seek over her body and along her gigantic limbs’. Modern research suggests that, at least amongst the orb weavers, it is more likely to be natural selection acting on the female, magnifying her body in the interest of maternity: a big momma is better equipped to withstand the excessive burdens of spider motherhood.

Stephen Jay Gould was one of several doubters to note that the male’s tiny size – sometimes as little as 1 or 2% of the female – would render his intake meaningless. Like feeding a pea to a hungry elephant. But in a cunning experiment in which some dark fishing spider females were prevented from cannibalizing the male, some were allowed to eat the male and some had the male switched out and replaced at the last minute with a cricket of the same size. The results of their study were conclusive: females that ate their lover had bigger offspring with greater survivorship. What’s more, the cannibalistic spider mums did significantly better than those that ate a cricket, suggesting it’s not just about the calories; there must be something uniquely nutritious about eating the male.

Just as the promiscuous female lion, langur and dunnock are not being wanton, but actually assiduously maternal and simply trying to do the best for their kids, so the female sexual cannibal is similarly merely protecting her future offspring’s best interests.  Sexual cannibalism has been shown to benefit one or even both of the sexes. It likely evolved independently numerous times in different taxa for different reasons, and is maintained by a cocktail of selective forces: as if sexual conflict, sexual selection and natural selection got drunk together and had a very messy night.

We know almost nothing about female reproductive organs but a helluva lot about penises

The widespread use of penis morphology in taxonomy means that there is more known about the male genitalia of many (perhaps even most) animal species than about any other aspect of their anatomy, behavior or physiology. So standard is the practice of genital identification amongst entomologists that an army of insects, such as Cacoxenus pachyphallus, the ‘thick dick’ fly, have found themselves named after their privates for easy ID.

Science has amassed a robust literature on penile variation, with intricate drawings and exhaustive descriptions, some dating back over a century. Yet when it came to the female counterpart there was almost nothing to be found. This gaping hole in genital research was little cause for concern, however. The general opinion held that female genitalia were little more than simple tubes that received ejaculate – passive and immutable with no cause to influence evolution, much like their owners.

Opossums are amongst the animal kingdom’s most accomplished actors; their flair for playing dead has evolved into a multi-sensory performance that includes not only lying stone stiff for hours on end and frothing at the mouth but also emitting a green anal slime that positively reeks of death. In reality opossums don’t die easily – they are immune to pit viper venom, allowing them to dine on otherwise deadly snakes, and they also appear to be impervious to botulism and rabies. They have opposable big toes that act like thumbs, crowded mouths that contain no less than 50 teeth, and the female sports 13 nipples in her pouch to suckle 13 undercooked babies each the size of a bee.

Early naturalists were blindsided by the opossum’s penis, which has the unlikely appearance of a fleshy two-pronged fork. They looked for a pair of holes to receive this twin-branched tool, and settled on the animal’s nostrils as the logical point of entry. Had anyone bothered to look inside a female opossum they would have discovered an equally bizarre bifurcated system involving two ovaries, two uteri, two cervices and two vaginas. What makes this embarrassment of riches even more extravagant is the arrival of a temporary third vagina which emerges for the sole purpose of giving birth and disappears shortly afterwards like a secret door.

The greatest difference between humans and our closest relative the chimpanzee, for example, is not the size of our forebrains, the arrangement of our teeth or even the flexibility of our digits. It is our genitals. The chimpanzee penis has no glans or foreskin, is held firm by a bone and as a final flourish its surface is sprinkled with hundreds of small spines. The human penis is a humdrum fleshy tube by comparison: thick, blunt, boneless and (thankfully) spineless.

No body part evolves as fast as genitalia. This implies they must be under some powerful selection forces. But for centuries the science of studying genitals was not considered a seemly focal point for scientific enquiry. It was fine for the lower regions to be catalogued by taxonomists as part of their perfunctory inventory of physical life, but nobody probed the folds for evolutionary explanations as to why such wanton creativity had arisen in the first place.

Darwin is partly to blame. In The Descent of Man, and Selection in Relation to Sex, he insisted that the creative exuberance of sexual selection didn’t act on genitalia. He considered sex organs to be primary sexual characteristics – survival essentials and therefore under the utilitarian guidance of natural selection alone. Sexual selection only acted on secondary sexual characteristics – unessential frivolities such as bright plumage or unwieldy antlers; the sexual dimorphisms involved in either male–male competition or female choice.

Salvation arrived, a full century later, in the form of a microscopic penis shaped like a brush. The year was 1979 and Jonathan Waage, an entomologist from Brown University, quietly published his succinct observations on the sperm-scooping, as opposed to delivering, talents of the damselfly penis. Brown demonstrated that the rows of stiff backwards-facing hairs at the tip of the phallus enabled the male to spring-clean the female’s reproductive tract, removing any lingering sperm left by rival males

How birds do it

Avian sex generally takes place using a multifunctional unisex hole called a cloaca. The male and female evert and momentarily touch cloacas in what’s known as a ‘cloacal kiss’. The brotherhood of birds that buck the trend by having a secret penis stored in the entrance to their cloaca, which unfurls only during sex, represent just 3 per cent of all bird species. Joining the tinamous in this exclusive avian penis club are emus, ostriches, ducks, geese and swans.

Some 66-70 million years ago the Neoaves, which includes over 95% per cent of the world’s birds, somehow lost their penis. This seems careless at best, but evolution must have its motives. Penis loss was a weight-saving device for flight. Or perhaps not. A female perspective offers a different explanation to the traditional phallocentric weight-saving theory. The loss of the Neoaves’ penis is the product of female choice. Females have chosen less coercive males with smaller penises and, over millions of years of this selective bias, the penis eventually disappeared. 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.

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. With twice the parenting, offspring can hatch earlier and females can have bigger and more frequent clutches, giving the penis-free Neoaves – the most successful of all the bird lineages – their evolutionary edge.

Though ducks have penises, amongst the longest in the vertebrate kingdom proportional to body length. The Guinness World Record holder is the diminutive Argentinian lake duck (Oxyura vittata) whose penis, when fully erect, is 42.5 cm long (almost 17 inches) – a full 10 cm longer than its modest body. It also corkscrews counter-clockwise and has a base covered in tiny spines.

The penis of the duck, like the antlers of a stag, is a seasonal event. For most of the year a duck’s penis shrinks to a tenth of its size and only during the breeding season does it grow, in some species almost exponentially. When not in use it is tucked away discreetly. When the drake is poised to penetrate, he pumps lymphatic fluid into his member, and the penis explodes out of his cloaca at 75 mph, unfurling itself in a third of a second like some kind of sinewy party hooter. 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. Males can win females by courting them using baroque displays involving ornamental feathers and funky acoustics sculpted to an aesthetic extreme by female preference. These displays can start months before the breeding season, giving the female plenty of time to select the father of her ducklings.

Those males left partnerless take a darker path to parenthood by engaging in forced copulations. In many duck species lone males band together to ambush and force themselves, en masse, on defenseless females. Amongst mallards 40% of copulations are forced. In such competitive situations the theory goes that the longer the penis, the more chance a drake has of getting his sperm closer to the egg and winning the race. Which means that in this particular battle of the sexes, the female duck is an abused loser. Not only is she the victim of assault by a ballistic weapon but, more importantly, she’s robbed of her sexual autonomy. The female duck no longer gets to choose which male fertilizes her precious eggs, which is the ultimate evolutionary blow.

Female mallards are not alone in being prey to coercive sex. Across the animal kingdom males have evolved myriad ways to win and control paternity, whether the female is consensual or not. Insects called water striders (various Gerris) have hooks which latch on to the female and prevent her from escaping copulation. In one newt species the males massage sneaky hormonal secretions on to the skin of the females they are courting, which act as aphrodisiacs.

Textbooks say duck vaginas are little more than simple tubes, but the female’s reproductive tract is just as complex as the male’s. It is not only long and littered with blind pockets but it also spirals clockwise – in the opposite direction to the male’s penis, and seasonal.  Although over a third of duck mating’s are forced, only 2–5% of ducklings arise from these invasive copulations.

The species with the longest penises correlate with those where the female piping has a twisty-turny obstacle course, and forced copulations were rife. In monogamous territorial species like swans and Canada geese the male’s penis was a much more modest affair and the female’s vagina correspondingly simple. So clearly male and female genitals must have co-evolved antagonistically in some ducks. Scientists believe that the female can actually select which drake fertilizes her egg by permitting the passage of his penis further into her oviduct. In non-forced situations, drakes will woo the female with their pre-copulatory dance. If the female wants to mate she adopts her receptive posture, lying flat in the water and lifting her tail. 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 female earwig has storage organs for sperm, so males can’t sweep out all other males sperm, so the female retains control of paternity.

People had presumed the folds in the dolphin’s vagina evolved to protect the uterus from the harmful effect of saltwater, which can be lethal to sperm. But dolphins are essentially like ducks in their genitalia. This is especially interesting, as dolphins have another key thing in common with ducks: forced copulations.

Recent work has shown that when male eastern mosquitofish evolve longer genitals (known as gonopodium) to harass females with, females grow bigger brains in order to outwit their aggressors.

The clitoris is perhaps the only organ more understudied than the vagina

It arrived on the anatomical map in the mid-16^th century, ‘discovered’ a bit unconventionally by an Italian Catholic priest called Gabriele Falloppio (1523–62). When Falloppio’s finding was shared 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 only in hermaphrodites. This inglorious misunderstanding set the stage for the next 450 years, which saw the clitoris routinely lost, rediscovered and subsequently dismissed by the medical patriarchy.

In many manuals the clitoris was present in the early 1900s, and subsequently deleted mid-century, suggesting that its omission was perfectly intentional – a subconscious means of denying women sexual pleasure, perhaps. The anatomical bible Gray’s Anatomy was just one of many to remove the clitoral label from their diagram of female genitalia. Other textbooks significantly undersold the clitoris’ size, the extent of its nerve supply, or only deigned to mention the external glans, accompanied by a cursory explanation of its form being merely a ‘small version of the penis’

But all vertebrates have a clitoris.  Female bonobos, our closest ape relatives, have a clitoris that’s positioned to facilitate mutual stimulation with other females. In humans the clitoris sits outside the vagina, which seems rather inconvenient when you know that in the majority of mammals the clitoris is positioned inside the vaginal entrance, where it can be easily stimulated by the penis during sex.

This is the case for the bottlenose dolphin. A combination of this vaginal position and the enlarged size of the dolphin clitoris screams sexual pleasure. The existence and role of such desire in female animals has long been controversial, but is logical. Sex, like eating, is essential for life. So, why should it not feel good?

It turns out even female insects enjoy sex, if it is done right.

It’s likely that female genital stimulation in mammals acts as a form of copulatory courtship, to induce ovulation or aid in the transport of sperm. In which case, a measure of pleasure might be another way a female subconsciously decides if a male gets to fertilize her eggs or not.

Danish pig farmers know all about this. They’ve discovered that artificial insemination is more effective if preceded by manual stimulation of the clitoris, cervix and flanks. So they’ve taken a practical approach and developed a special five-step sow stimulation routine, with graphic images for guidance. Seduction starts with the farmer stimulating the sow with a fist, moves on to massaging her hips and finishes with the farmer sitting on her back to mimic the weight of the mating male on her. This sow seduction formula results in 6% more babies than going in straight with a cold hard syringe, but may put some off a career in pig farming.

Despite their image as racing Olympians, sperm don’t actually have the energetic resources or directional swimming skills to travel under their own steam to the site of conception. They need help. In some primates the degree of sperm uptake has been linked to contractions associated with female orgasm. During climax, the release of the hormone oxytocin causes the uterus and oviducts to contract resulting in the ‘upsuck’ of sperm, which significantly accelerates their passage to the egg. A study of captive Japanese macaques, Macaca fuscata, found that females are more likely to achieve orgasm-like responses when mating with high-ranking, socially dominant males, suggesting preferential sperm uptake for these males.

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. Unfortunately, although recognized for more than 50 years, capacitation remains an ill-defined process.

Does the ova pick the winning sperm?

Ova have long been considered the very epitome of female passivity; their large size and sedentary nature, in comparison to the small and mobile sperm, the very source of sexual inequality. Textbook descriptions of fertilization take the form of a biological fairy tale, with the helpless princess ovum waiting listlessly for her heroic sperm prince to battle his way to her rescue and awaken her from her lifeless slumber. But there is growing evidence that the egg can actually influence which sperm gets to enter, regardless of which one ‘won’ the race. Unfertilized eggs are known to release chemo-attractants that essentially leave a trail of biological breadcrumbs to guide sperm in the right direction. Not all sperm react in the same way, meaning there is room for the egg to select the optimal candidate, rejecting those that are genetically incompatible even if they arrived first. The egg makes no concessions for romantic partners, however. In the study of human eggs, in over half of the cases the egg preferred the sperm of a random male and not the woman’s partner.

Of the dozen or so species of primate in the rainforest, the black-headed owl monkey wins the prize for being the most enigmatic. These miniature primates, roughly the size of a small squirrel, hide out high up in the canopy and aid their secrecy, as the name suggests, by being the world’s only nocturnal monkey. They live in family groups and are, unusually for primates, monogamous. Pairs will have just one baby a year – a ball of dense fluff that fits in the palm of your hand and could have been pumped out of a Japanese kawaii factory – all eyes and devastatingly cute.

Motherhood

Muqui was calmest clinging to a mass of hair, which made the prospect of potty-training especially onerous. He slept pretty peacefully atop someone’s head during the day, so much so it was easy to forget he was there until you bent over and remembered you had a (now screaming and quite possibly urinating) baby monkey clinging on. Night-time Muqui became an altogether different beast. His behavior was electrified, and we took turns in babysitting the super-charged night owl.

After he’d been at the station for a couple of weeks, night-nurse duty fell to me. This is what I wrote in my diary the following day. I have to sleep on my front with Muqui nestled on the back of my neck under my (long) hair. He wakes 4–5 times in the night for milk by clambering on my face and rubbing my ear. He must pee and poop after his feed but it is impossible for him to take on board that he must leave the confines of my bed to do so. He prefers to return to my (increasingly) bird’s nest hair, which is far from ideal. Generally he is getting bolder – exploring all night by running over my body and frantically climbing inside the mosquito net. Activity peaks around four a.m. with a frenzy of ear rubbing and hair exploration. This morning I look like Robert Smith of the Cure. According to Darwin, this should all have been second nature to me. My maternal drive should have kicked in and transformed me into an intuitively wise and selfless nurse. But the truth was I felt quite traumatized by the experience – fretful, out of my depth, exhausted and, for the sake of my defiled and defecated-on hair alone, uninclined to repeat the whole sorry ordeal ever again.

Female animals have long been equated with mothers as if no other role existed. Motherhood is an emotive subject – synonymous with nurture and sacrifice; and, as such, riddled with misconceptions, the most fundamental being that all females are born ‘natural’ mothers, imbued with an almost mystical maternal instinct that drives them to effortlessly intuit their offspring’s every need. The most obvious problem with this idea is it assumes caring for young is the sole responsibility of the female. In Muqui’s case, his mother would have suckled him every few hours. But after each feeding bout she would have driven him away, quite unsentimentally, by biting his feet or tail, leaving his father to take on the role of primary caregiver and the heavy job of carrying him 90% of the time.

Infanticide is also common amongst mammals – having been recorded in around 60% of species. Male mice routinely kill babies that are not theirs, but won’t if they are the father. Mothers, on the other hand, will sacrifice their own babies if they become heavily stressed – by predators or hunger.

It makes sense that the compulsion to parent must be equally hardwired. Animals are fundamentally concerned with their own survival, and rightly so. Theirs is a life-or-death world, in which the struggle to eat or not be eaten is a daily deadly reality. Why would a female mouse take care of a little pink thing that suddenly arrives, screams a lot and is very demanding? Having to handle it and make sacrifices is extremely dangerous. This is where parental instinct is kicking in. It says you have no choice but to care.

You and I are alive today because some of our ancestors used their galanin cells to nurture our ancestors, but also because there were these urocortin cells that allowed mum to decide whether it was a good time to have babies or not. Without them she might have died.

Infanticide is strictly pathological in humans. We are part of the 40% 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.

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.

Most adult females in most animal populations are likely to be breeding at, or close to, their capacity to produce or rear young, wrote the standard textbook, as if to see one mother was to see them all. Natural selection requires variation in order to function, which means mothers were effectively barred from the evolutionary party on account of being too boring.

Altmann developed a method of sampling subjects at random and made sure each individual was watched for the same number of minutes – because statistically all behavior is of equal importance, however ‘boring’ it may seem to be. The resulting paper outlining her methodology, ‘Observational Study of Behavior: Sampling Methods’, was nothing short of revolutionary, for ever changing the face of field research, not just in baboons, but across the animal kingdom. Cited over 16,000 times to date, it’s been described as one of the greatest feminist papers of all time, since it finally gave females the same airtime as males.

Altmann knew she needed to collect data on the same groups of animals for generations in order to calculate the ramifications of their behavior in deep time. She chose savannah baboons.  Her  landmark study, which continues to the present day, forged new ground by ignoring the lavish spectacle of competing males that so transfixed mainstream science and focused instead on mother–infant relations. It was a courageous career move. Mothers considered to be of little theoretical significance to the mostly male zoological establishment. At over 50 years old, it is the longest-running primate study in existence. The accumulation of almost seven generations of unprejudiced observational data on the lives of over 1,800 individual baboons has transformed our understanding of not just the species but mother-infant relations in general.

This research revealed that every baboon mother juggles the demands of a ‘dual career’. She must spend 70% of each day ‘making a living’ – foraging, walking, avoiding predation – while at the same time managing the job of caring for her infant. Baboons travel several kilometers 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 other tree limbs. If the infant isn’t carried just right, it can’t suckle and can quickly dehydrate and die.

Mastering this technique can be especially challenging for first-time mums, who are often ‘puzzled’ by their infant’s distress. The trigger to parent may be hardwired, but maternal behavior unfoldes gradually and there is much for first time mothers to learn. Amongst primates, mortality rates for first-born infants are up to 60 per cent higher than subsequent siblings.

Even amongst experienced baboon mothers infant death is a very real threat. Altmann discovered that 30–50% of babies perish within a year, with nutritional stress being a key culprit. Food is scarce on the dusty plains of Amboseli, the environment unforgiving and unpredictable.

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 is independent from one to two years old.

Baboons, like all mothers that breed several times during their lifetime, must balance the investment in their current offspring against their own survival and future reproductive capacity. The average baboon is likely to spend 75% of her life having babies – around 7 in total, with only two likely to survive to adulthood. So baboon mothers are pushing the envelope of their own survival – if they were to bred any faster they would risk dying themselves.

Not all mothers are born equal, however; a female baboon’s lot in life is strictly dictated by her social class. Females also inhabit their very own chain of command – a rigid female aristocracy, worthy of the British nobility. Status is immutable and inherited – passed down the maternal line – and laced with privilege. Those females lucky enough to inhabit the upper echelons have first dibs at food and water sources, they can displace the hoi polloi to get groomed, and generally enjoy the freedom to go wherever and do whatever they want, including snatching and even kidnapping other females’ babies.

Low-ranking mothers are especially vulnerable. They lack the social standing to be assertive so high-ranking female daughters can just grab their baby, and when they get bored of playing with their new toy they abandon it, which can be heartbreaking to watch.

Daughters born into baboon nobility have the advantage of their mother’s social connections, which turns out to be the greatest gift of all. This wide network of benevolence offers protection from the threat of kidnapping females or infanticidal males as well as the competitive aggression of other baboons. High-born, well-connected infants are more likely to be tolerated when feeding nearby another adult. This support system means mothers don’t have to be the be-all and end-all for their kids, which is especially helpful for first-timers surfing a brutal maternal learning curve. Altmann found that daughters surrounded by high-ranking kin give birth at an earlier age to offspring more likely to survive, giving them a lifetime reproductive advantage over mothers in the lower ranks.

This social privilege, or lack thereof, has a massive impact on a baboon’s mothering style. Noble-born mothers have what Altmann described as a ‘laissez-faire’ approach to the job. They have the confidence to let their infants roam far and wide, and exhibit tough love early on when it comes to weaning. This hands-off approach makes for self-sufficient and socially integrated juveniles, which gives them a higher chance of survival as adults.

Low-ranking females are put upon by just about everybody. Without the social standing to protect them and their baby, they compensate with what Altmann describes as ‘restrictive’ parenting, keeping their infant constantly within arm’s length. Restrictive mothering probably results in a better initial survival rate, as the infants are safer from predation and disease in the first few weeks. But they develop independence more slowly and place more demand on the mother’s critical resources, pushing her closer to that energetic cliff edge, and death.

Faced with a non-stop stress-fest of potential threats, 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 feces, is thought to lower their immune response and make mothers more vulnerable to disease. There are ways they can cheat the system and give the next generation a better chance of survival, such as forging strategic friendships with other baboons, either male or female to gain much-needed assistance when running the brutal Darwinian gauntlet.

Females who have friends live longer and their kids survive better. The ability to forge strong and enduring social bonds may even generate more reproductive benefits than high rank.

Baboon mums have another destiny-cheating tactic: they can unconsciously manipulate the sex of their offspring. Low-ranking females had more sons than daughters. This plays to their advantage. Female status passes down the maternal line and is fixed, so low-ranking daughters remain shackled to the disadvantage of their mother’s miserable status for life. Male baboons, on the other hand, fight one another to dominate their hierarchy, so their status is more fluid. Plus a son who manages to hitch his reproductive star to a more successful matrilineage can score a high-class daughter to secure posterity for his offspring and escape low-class purgatory. So, if you are a low-status mother it makes sense to produce sons who have a chance to escape the confines of a nepotistic line instead of daughters, who are trapped.

In contrast, high-bred female baboons produce more daughters than sons. Since their privilege is assured, daughters are a less risky gamble and, Altmann observed, have a higher chance of survival than high-born sons.

Bird mothers can micromanage the hormonal and nutritional contents of individual eggs to give certain siblings an advantage over others. Mammalian mothers can tailor their milk to fit their offspring’s specific requirements. Macaque males, for example, get a shorter burst of richer, high-density milk, whereas females get weaker milk but are nursed longer. Rich milk may help sons bulk up faster and have a competitive edge as adults.

Abortion is a natural strategy    

Exactly how baboon mothers, be they low- or high-ranking, manage to fix the genetic deck in favor of the ‘right sex’ isn’t yet clear. But in other sex-manipulating mammals, like coypu and red deer, their method is strategic abortion. The idea of a female taking such brutal command of her reproductive destiny may not be welcomed by the pro-life brigade. The uncomfortable truth, however, is that nature is decidedly pro-choice. Abortion, at every stage of pregnancy, is an unconscious adaptive strategy for many animal mothers facing unfavorable situations that put them or their offspring in peril.

In the wild, gelada baboons will abort when a new dominant male takes over the group. Incoming males almost always kill any babies they didn’t sire, so terminating the pregnancy is a mother’s insurance policy against this almost inevitable infanticide and wasting any further reproductive effort on a likely dead end. This trigger for abortion has since been documented in all sorts of wild animals.

The goal of motherhood isn’t to nurture babies indiscriminately but for a female to invest her limited energy in creating the maximum number of offspring that survive long enough to reproduce themselves. There is nothing truly selfless about the job; it is absolutely selfish. A ‘good mother’ instinctively knows when to sacrifice all for her offspring and when to cut bait, which might even be after the infant is born.

Pandas, kangaroos, and many other animals also can abort when conditions aren’t good for raising babies or to save her own life.

Motherhood may be energetically demanding, but viewed another way, that high price tag offers female mammals far more control than males in shaping their precious genetic investment. Viewed from this alternative perspective, far from being irrelevant, mothers actually make a greater evolutionary impact than fathers. And that gives them greater power too in choosing which infants survive, unconstrained by motherhood in difficult circumstances.

Oxytocin

Oxytocin is fundamentally involved in the actual physiological process of becoming a mother. It acts as a smooth muscle contractor, which, in mammals, stimulates the uterus to pump out babies as well as the nipples to eject milk. The physical process of labor 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.  This flood of oxytocin rewires a mother’s brain, tuning it to the cries, smells and sight of her offspring. It seems to make social information more salient by connecting brain areas involved in processing social information – whether it’s faces, sounds or smells – and those areas to the dopamine reward system. So when her baby cries for the hundredth time, a mother will be motivated to respond by the delivery of yet more natural opiates.

Lactating mothers are certainly drunk with the stuff, which could explain their heroic levels of self-sacrifice. Mothers can be famously fearless when it comes to defending young – ‘never come between a mother bear and her cubs’, as the old adage goes. This heightened ferocity is unique to nursing mothers, and the so-called ‘cuddle hormone’ has been implicated in their Jekyll and Hyde transformation. Oxytocin is thought to reduce anxiety and fear, helping a mother cope with maternal stress and priming her to valiantly defend her offspring against any potential threat.

Oxytocin levels provide a reliable metric for predicting maternal behavior in wild grey seals: mothers with high levels spend more time snuggling up to their pups and developing a strong attachment. Low oxytocin levels suggest a less secure bond.  Also, it seems that for mammals that recognize their young by smell there is a critical window, a few hours immediately after birth, when the brain’s olfactory bulb has a heightened sensitivity and the mother–pup bond is cemented. If the mother gets distracted during this critical period, say by chasing off a seagull that’s scavenging on her freshly birthed placenta, then oxytocin levels can remain at the level of a non-breeding female. If for any reason they miss that bonding window, you can’t recreate it outside of giving birth or having a massive artificial dose of oxytocin injected into your brain. And that’s when you start to see these rejections of the baby.

Fortunately, the biology of maternal bonding doesn’t only rely on a precarious rush of oxytocin following birth and lactation. Evolution has ensured there are other longer and more secure roads to attachment, which make caring for babies a more egalitarian arrangement.  Humans and rats will foster unrelated young. Adoption has been recorded in at least 120 mammals from elephants to shrews.  Although caring for and provisioning someone else’s offspring seems at first to defy evolutionary logic, cooperative breeding has evolved many times in a taxonomically diverse array of species. Around 9% of the 10,000 living species of birds and 3% of mammal mums get much-needed help from what are referred to as allomothers, literally ‘other mothers’.

It wasn’t hunting and warfare, but shared child-rearing in tribe that made us human

Whereas Darwin proposed that provisioning by increasingly skillful male hunters subsidized our leisurely development, leading to the evolution of ‘greater intellectual vigor and power of invention of man’, Hrdy believes that, much like the black-and-white ruffed lemurs, a less gender-specific gaggle of helpers was around to share the caring load. And this maternal help was the real key to our extraordinary intellectual advancement.

An orangutan mother gets no help and as a result can only afford to have a baby every 7-8 years. By contrast the interbirth interval for a human hunter-gatherer is just 2-3 three years. Shared guardianship favored 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.

Why females fight each other over male sperm

In Darwin’s reading of the animal kingdom, females have no need to fight over sex. But contrary to the wishful beliefs of Darwin and other evolutionary biologists, sperm supplies are far from cheap and limitless. For example, Topi females fight violently over the finite seminal supplies from the most sought-after members of the opposite sex. Some pushy cows even went so far as to charge top studs in the act of mounting other females. The goal of the males is to mate with as many females, deliberately choosing the females they have mated with the least to maximize their chances in sperm competition.

Recent research on western lowland gorillas supports this. Studies on both wild and captive populations found the females in a silverback’s harem compete with one another using sex itself as a weapon in the sperm wars, probably because silverbacks have notoriously small testes for their body size, suggesting limited supplies. In captivity, high-ranking females have been observed having sex outside of estrus, when there is no chance of becoming pregnant, in order to raid the silverback’s semen stores so he only shoots blanks into her low-ranking love rivals. In a wild population in the Congo, high-ranking female gorillas were seen to be even more audacious: harassing, interrupting and even replacing lower-ranking females during copulations.

It’s assumed females aren’t competitive, and theories are based upon that understanding – when the truth is we just haven’t been paying attention. Birdsong is a case in point. The melodious calls of songbirds have long been considered a classic example of sexual selection: a male ornament that evolved to be ever more elaborate in order to successfully compete with rivals to win the affections of the opposite sex. Birdsong might not seem costly, but memorizing all those songs requires a bigger brain, which is both energetically and physically expensive for a small creature that flies for a living. In fact, the male songbird’s brain is known to shrink in the winter months when he’s not required to sing.

Any female songbirds caught singing were written off as babbling freaks. The accepted wisdom was if you hear a female sing, it’s a functionless aberration – an old female that has a bit too much testosterone in her system. But 71% of female songbirds sing, proving that female song wasn’t some recent evolutionary kink, found only in the tropics. Female songbirds had always sung. What’s changed is that, in some northern temperate regions, in the more recently evolved families of songbird, females have, for some reason, ceased singing.

The question we should really be asking is not why do male birds sing, but why have some females subsequently lost song? 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.

There’s a real role for the female to defend her territory because the male may die, he may divorce her, or be sneaking copulations next door with another female. In any of those circumstances, the female still has to be able to defend her territory against any intruders, and perhaps even sing to attract a new mate. So in these tropical regions, it’s very valuable for a female to be able to sing,’

It’s a very different scenario in the gardens of Europe or North America, where most of the songbirds migrate south in the winter. When they return the male generally arrives first and sings his head off to establish a territory and attract a mate. Females will shop around before choosing a male, which has, in some cases, resulted in elaboration of male song through sexual selection. The breeding season is short, however, so she has to get down to business and breed before she packs up to move south again. As a result she’s less likely to be getting into fights with other females and selection for song has been relaxed.

Birdsong is clearly as adaptive for females as it is for males. Cunning experiments have even shown that migratory females that rarely sing, like American yellow warblers, can be induced to start singing if other females, albeit dummies, muscle in on their territory.

Female hierarchy

When it comes to social species, status is key for determining access to food, shelter, top-quality sperm – all the resources a female requires to reproduce. So it pays to be the top bitch. Males may suck up all the attention with their bloody battles for supremacy, but group-living females generally inhabit some kind of hierarchy, often independent of the male order. The first dominance system ever fully documented was, in fact, feminine in nature. A young Norwegian scientist by the name of Thorleif Schjelderup-Ebbe introduced the scientific world to the very first alpha, which just happened to be a female chicken.

He noticed that during routine squabbles between pairs of hens in a group, one would peck the other. The pecker, generally the older of the two, would henceforth gain priority access over the loser to the best roosting sites and food. Following rounds of pecking contests, an overall champion would emerge and group aggression would cease, as each bird understood and accepted her place in the resulting hierarchy. The top-ranking hen, which he named the ‘despot’, would however routinely remind any subordinates daring to eat before her of their relative social status by administering a painful peck.

Schjelderup-Ebbe had recognized that female hierarchies were far from trivial. ‘Fights among chickens, which are usually considered to be quite harmless, are certainly not so and do not result from a momentary whim,’ he wrote. ‘They put a lot at stake, sometimes even their lives, in order to win.’

This is true across animal societies, from birds to bees. The prize for clawing up the social ladder to alpha female status is a significant reproductive advantage, and it’s worth fighting for.

In males the battle for supremacy can be bloody and boisterous and hard to ignore. Female power struggles are generally far subtler, although no less devastating. Which is probably why many female hierarchies went largely unnoticed for decades.

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. A low-ranking female baboon’s best chance of survival is to play a deft political game and ascend the social ladder through strategic coalitions that protect her and her offspring. Female primates have been described as ‘obsessed with signs of status differences or disrespect’. They just don’t make it as obvious as the males.

Meerkats live in clans of 3 to 50, with a single dominant female monopolizing 80% of the breeding. The rest of the mob – her relatives, descendants and a few itinerant males – help out with territorial defense, sentinel duties, burrow maintenance, babysitting and even suckling the dominant’s pups. This kind of division of labor, where only a few individuals get to breed and the rest of the group helps, is known scientifically as ‘cooperative breeding’

This term has always struck me as wildly euphemistic. The meerkat’s apparent camaraderie isn’t achieved through cozy cooperation so much as outright tyranny. Meerkat society is predicated on ruthless reproductive competition between closely related females who, when pregnant, will readily kill and eat each other’s pups. This baby-eating bonanza is kept in check by the omnipotence of a dominant female with a zero-tolerance policy for breeding subordinates. Her goal is to prevent any of her female relatives reproducing during her reign, and rope them into caring for her babies instead. This removes any unwanted competition for her pups and protects them from being eaten. It also allows her to invest all her energy into raising more litters than she could do otherwise. It’s a prize position that’s worth fighting hard and dirty for.

Vacancies for dominance don’t come up often. Generally the position only becomes available when a matriarch dies, perhaps at the talons of a hawk or a rival meerkat gang. The top job then falls to the oldest and heaviest female in the group, most likely one of the matriarch’s daughters. From the moment a meerkat inherits her supreme status her size increases, her testosterone levels rise and her hostility towards all other females will surge. She will demonstrate particular hostility towards those that are closest to her in age and size – most probably her sisters – and who therefore make up her greatest reproductive competition.

If you are a female meerkat your best bet – your hope in life – is that someone will eat your mother. But it’s no good if they eat your mother at the wrong time. What you really want is for them to eat your mother when you are the oldest subordinate in the group. Otherwise one of your bloody sisters gets the job and she throws you out. You regularly see dominant meerkats evicting their older daughters. They are brutal: if their daughters don’t get the hell out, they kill them. If you look at a meerkat group there are basically no subordinate females over 4 years old because the dominant females evict them between the ages of 2 to 4.

Next comes physical abuse: hip-slamming and the casual biting of tails, necks and genitals are all favored moves by a dominant female looking to exert her power. Corporal bullying serves to impose authority and, as an added bonus, the resulting stress could also depress the victim’s fertility. Its main purpose, however, is to make life so unpleasant for the victim that they will leave the group.

Exile may sound like a walk in the park compared to a constant barrage of snack swiping and genital biting. But the only thing more oppressive than a dominant female meerkat is the Kalahari Desert itself.  Environments don’t come much less forgiving than this vast semi-arid savannah. Rainfall is a hazy memory for most of the year and temperatures fluctuate by 45 degrees Celsius daily (113 F). During the height of summer the daytime temperature tops 60 degrees Celsius (140 F), yet in the winter the nights can be freezing. Without warm bodies to huddle next to in a communal den, a meerkat could easily go to bed and never wake up.  If a rival gang of meerkats doesn’t kill an exiled female, there are dozens of sharp-eyed predators only too eager to turn a lonely meerkat into dinner. The soft sand that meerkats need to forage in is only found along dry river beds, grasslands and dunes with little or no vegetation for cover. That leaves a hungry meerkat highly exposed – out in the wide open, digging away with their head in the sand. Without a sentinel to keep watch and sound the alarm for predators, a solitary meerkat is easy picking for umpteen aerial predators, wild cats or jackals.  It is the brutality of the Kalahari that gives a reproductive autocrat the necessary leverage to enforce her totalitarian regime.

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.  They may be permitted to slink back to the group on one condition: they take up wet-nursing duties for their murderous mother’s babies. Suckling is a serious drain on a subordinate’s reserves, but these enslaved females have no choice when the alternative is exile and a lonely death.

Meerkat culture is tense and homicidal. A study investigating lethal violence in more than 1,000  different mammals unmasked the meerkat as the most murderous mammal on the planet – beating even humans to the brutal top spot. Every meerkat born has a one in five probability of being killed by another meerkat, most likely a female and quite possibly their own mother.

Termites

The queens of the co-op life are, of course, the social insects – namely all species of termite and ant, as well as some wasp and bee – whose societies are a wonder of procreative totalitarianism. Only one in tens of thousands of females ever get the chance to become a mother. Those that do can be extraordinarily productive since their sole job is to lay eggs.

Those belonging to the species Macrotermes bellicosus not only farm fungus but also create towering humidity- and temperature-controlled mounds up to nine meters tall on the savannahs of West Africa. At their center is the royal chamber. Unlike with ants and bees, this includes both a queen and a king, who mates with her for life. In many species the queen swells into a monstrous egg-laying machine whose abdomen has swollen over a thousand times into a giant waxy off-white sausage around ten centimeters long. Her head, thorax and legs remain tiny and can only flail about pathetically, since all other movement is restrained by her grotesque, pulsating girth. She must be fed and her gargantuan maggot-like body cleaned by a legion of workers, allowing her to spend every bit of her energy squeezing out a fresh egg every three or so seconds, all day every day, for up to twenty years. At over 20,000 eggs a day, she’s capable, in theory, of producing some 146 million termites in her lifetime, making her the most reproductively successful terrestrial animal on the planet.

This extreme brand of cooperative breeding, involving such a clear division of reproductive labor between breeders and infertile working castes, is known as eusociality – from the Greek eu- meaning ‘good’. Although this is another highly subjective term since, in truth, it is only really ‘good’ for one individual: her Royal Reproductiveness.  All of which makes the British monarchy suddenly seem quite reasonable.

Naked mole rats are truly exceptional-looking creatures that regularly top the ugly animal charts. They look like a penis with teeth. The naked mole rat’s face is one only a mother could love – if only the mother in question were not a highly belligerent despotic queen with no love for anything. Their wrinkly pink body is indeed remarkably phallic, and protruding from the tip of a helmet-like head are two pairs of terrifyingly long yellow teeth. These are especially prominent since the mole rat’s lips close behind their ever-growing gnashers so they don’t end up choking on soil while they use them to dig. With little more than two black dots representing their useless representing their useless eyes and no external ears, the overall effect is indeed the-Johnson-from-hell, somewhat ironic for a female-dominant species.

The mole rat’s nude skin is stretchy and unbelievably soft to reduce damage from the abrasive nature of tunnel life. 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 elastic and may be why they don’t get cancer.

Naked mole rats are a true scientific wonder. The world’s only cold-blooded mammal, capable of surviving 18 minutes without oxygen and feels no pain. These almost indestructible rodents can live for over 30 years – eight times longer than expected for an animal their size.

Colonies are ruled by a single queen who does all of the breeding with one to three selected males. Four to five times a year she’ll give birth to around a dozen pups, though she can squeeze out more. In order to pump out this many babies, the queen’s body can become grossly distended, just like a termite’s. Like a social insect queen she also lives 10 times longer than the workers of the colony, but with no age-related decline in her fertility.

Other than the queen’s chosen mate, the rest of the colony act as workers or soldiers. Unlike in social insects, Faulkes tells me these subordinate roles aren’t hardwired, they’re plastic. The bigger mole rats tend to take on the soldier’s role of defense against invading foreign mole rats or predators like snakes, while the smaller ones are the workers and spend their days digging for tubers, sweeping the tunnels, tending to babies, or cleaning the toilet chamber.

99.99% of the colony will never reproduce. 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, the non-breeding castes are impossible to tell apart sexually.  How does she do this? Originally it was thought that, like social insects, pheromones were the answer, which the queen sprinkled around the colony in her urine like bromide in a soldier’s tea. Other researchers have suggested that subordinates are manipulated by eating the queen’s feces – they’re quite coprophagous. But for the queen to use faecal matter for such widespread colonial control would mean ‘shooting it out like a machine gun.

The answer is probably that both non-breeding males and females have really high levels of prolactin, which in humans is kind of instant infertility. Prolactin is high in pregnant women and new mothers – it stimulates the breasts to make milk and reduces fertility until the current offspring is weaned. So it is possible that there is a dual role of prolactin in mole rats: it not only stops them from breeding, but also makes them take good care of the colony’s young.

For the queen to maintain her dominance throughout the colony takes some serious legwork, spending enormous amounts of energy patrolling the colony. She is over twice as active as the next most active animal in the colony and travels three times the distance over 18 months. This relentless royal tour is necessary to maintain the colony’s sexual suppression. She’s not just lazily slopping around in the nest chamber and being fed by the others like a social insect queen. It’s a tough position because she has to maintain her dominance all the time.

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. When you play the game of thrones you win or you die” – that’s the famous quote and it really does apply to naked mole rats. They’re competing for the throne and they’ll kill anyone or die in the process. It’s super brutal.

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 fast. The extreme violence is down to the fact that, for the females involved, the vacancy offered by a weak or missing queen offers a once-in-a-lifetime opportunity to breed. Striking out alone is simply not an option in this netherworld. Naked mole rats can only exist as a self-sacrificing multitude. They’ve evolved to thrive in the most inhospitable environment imaginable by banding together, divvying up the tricky job of survival and sharing the load.

The Power of Sisterhood

In the movie Madagascar, the great African island is ruled by a fast-talking ring-tailed lemur called King Julien XIII.  The producers may have felt it only natural to impose male governance on their feel-good movie, but in ring-tailed lemur society females are unquestionably the authoritarian sex. 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, which has long been considered rare amongst mammals. The spotted hyena and mole rat matriarchs we’ve encountered in the book so far have evolved a significant size advantage, which allows them to reverse Darwin’s ‘natural order’ and overpower males. Lemurs show little in the way of sexual size dimorphism, however.

Spindly trees with branches aren’t strong enough to support a Sifaka lemur’s weight – roughly that of a cat. This makes travelling quadrupedally along branches or swinging from tree to tree like their monkey cousins out of the question. Sifakas have got around the problem by evolving oversized feet and hands to wrap around and cling to the trunks of the trees, and long legs for leaping. They do a brilliant job – the sifakas ping about like balls in a pinball machine as their powerful elongated thighs propel them up to 30 feet from one trunk to the next. Their locomotive system only exposes flaws when a sifaka is forced to the ground where their long legs, short arms and giant comedy feet make walking on all fours impossible. Instead they must bounce sideways, arms outstretched for balance.

Sifaka live in small family groups of around 2 to 12 individuals with a matriarch, her offspring and one or two adult males. The matriarch of the troop I met, known as Emily, was snuggled with her young at the top of the tree in a cozy huddle, in preparation for the chilly night ahead. Meanwhile Mafia, the adult male, was sitting below them – an oft-seen physical demonstration of rank – with no other body to cuddle than his own. Temperatures can drop to a brisk ten degrees Celsius (50 F) at night and frequently males are left out in the cold. Male sifaka are second-class citizens, forced to give up the comfiest, sunniest sleep spots and best food to the alpha female. Any resistance is met with a firm hand.

In a tropical forest so devoid of life, and so eerily quiet – no chirping insects, no birdsong, just the crackle of footsteps on dead leaves breaks the silence. There was clearly little for a leaf-eating lemur, or indeed any animal, to eat. ‘The sifakas lose 15 to 20% of their body mass in winter.  Baobab trees offer the sifakas an oasis of sustenance. These goliaths of the rooted world store water in their fat barrel trunks and, when the rest of the forest is all but deceased, they produce their fruit: green velvet balls the size of oranges containing lipid-rich, high-calorie seeds that dangle like Christmas baubles

The problem is that the fruit shell is hard and sifaka teeth are not. The male will spend forever gouging and gouging to get through this woody shell to the oily seeds inside, damaging their fragile toothcomb and when they finally get in the female goes whap, hits him across the head and says, “Thank you very much. I’ll take that!”’ I don’t know why the males stick around. They get beat up left and right, they don’t get the good food.

The aggressive dominance of the female lemur has troubled scientists ever since it was first discovered in the 1960s by a young American-born scientist named Alison Jolly, who died in England in 2014 aged 76. She is one of primatology’s lesser-known female visionaries. She pioneered a brand of environmental activism that helped protect much of Madagascar’s unique wildlife and established the idea that primate higher intelligence evolved to manage complex social relationships rather than toolmaking. This flew against the thinking of the time but is taken for granted today.

Jolly was the author of over 100 scientific papers, yet, despite such academic achievements, she was overshadowed by her contemporaries – Dian Fossey and Jane Goodall – and her contributions to science have somehow gone under the radar. Perhaps that was down to the heretical nature of her research. For while Fossey and Goodall were describing dominant silverback gorillas and the hierarchies of male chimpanzees on mainland Africa, Jolly was in Madagascar documenting something completely different – aggressive alpha females.

In ring-tailed lemurs, females that do the majority of territorial defense. They have well-developed scent glands and produce more chemical signals than the males – the reverse of what you’d expect. They seem to be more interested in the scent of their own sex than males, especially breeding females. The healthiest females produce a lot of fatty acid esters, which are a signal they are strong and sexy. Again, this is something normally only done by males. It suggests their scented signals are linked to competition with other females since males aren’t a threat and can be ignored. Females leave more marks in ‘confrontation zones’ and during battles between troops. When they stray into neighboring territory, they keep sniffing the scent marks of neighbors but don’t deposit their own scent, similar to what happens when male chimps go on ‘patrol’. When they go into neighboring territory they get very quiet so they don’t get caught. By sneaking next door and checking out the smell of the neighboring females, they can size up the competition, but by not leaving any of their own, they can do it surreptitiously, avoiding retaliation from the neighbors. If they do encounter anyone, they suddenly start scent-marking like mad, trying to scare off the others.

Female ring-tailed lemurs do get physical. They’ve been described as ‘exceptionally aggressive’ towards both sexes. They will terrorize and even evict subordinate females, which for a group-living species can be a death sentence. They show no mercy to mothers carrying babies, which often get killed in the crossfire.

Female hostility over rank isn’t unusual amongst primates – we’ve already witnessed bullying at play within the matriarchy of savannah baboons – but attacking males is. One study into female ring-tailed lemur aggression found that males are three times more likely than females to be seriously injured or even die from female violence. Ring-tailed lemurs are the only wild primates ‘where all females can be said to be dominant over all males’.

In the 60s and 70s primatology was hypnotized by showy male dominance systems. This obsession began way back when the science emerged in the 1920s. The zoologist Solly Zuckerman’s pioneering work on baboons (part of the Old World monkey line) set the tone. ‘Female baboons are always dominated by their males, and in many situations the attitude of a female is of extreme passivity,’ he wrote in 1932. Although Zuckerman’s colony was captive, overcrowded and unrepresentative of the wild, his observations grew into a theory that was to become a hallmark of primatology: the male dominance hierarchy is the defining principle of primate life. It governs access to resources (namely food and those ‘passive’ females) and is established by the ability to fight.

Following World War II, a preoccupation with the origins of human warfare quickly hijacked the emerging science of primatology. Later, in the late seventies, chimpanzees took over as the model for human ancestry. Jane Goodall’s revelations of their warlike nature fueled the idea that human males must be pre-programmed for violent supremacy, an idea made popular by the likes of Richard Wrangham, Harvard professor of biological anthropology and one of many influential male scientists to promote our primate ancestors as mirror images of chimps: patriarchal, male-bonded and highly aggressive.

Subsequent phylogenetic research has, however, revealed that Old World monkeys make for poor primate prototypes. Their behavior is actually highly derived, tailored to meet specific environmental challenges and far from representative. Primate societies in general are way more diverse than the familiar patriarchal model of baboons and chimps. But this natural diversity was overlooked – not just the lemurs but also the New World monkeys.

New World monkeys split from Old World monkeys some 40 million years ago in Central and South America like lemurs, aggressive male dominance is unusual. Most species are peaceful and egalitarian. The sexes are the same size and parental duties are shared. Where dominance is displayed, as in squirrel monkeys, marmosets and tamarins, it is the females which appear to have the upper hand.

How do female lemurs manage to get their way without the brawn to back up a threat? Lewis thinks that the source of a female’s power is obvious. She has something the male wants: an unfertilized egg. The female has this egg and she can say – you want to fertilize this? Guess what? If you want this, then I eat first. Lemurs have an especially short breeding season – in white sifaka it’s just 30 minutes to 96 hours a year, and in ring-tailed lemurs 4 to 24 hours. In terms of economics, if there’s only one female in estrus she should have a whole lot of power because short supply means high demand.

But as soon as you have just one or two females in heat at a time it incites males to compete to try to dominate this valuable resource. Males will evolve greater size and weaponry in order to fight off their love rivals, which, as a by-product, results in the kind of physical might that then allows them to dominate females, and subsequently reduce females’ egg-resource clout. So the same forces that allow the female more dominion also select for sexual dimorphisms in the male, which then physically undermine female power.

In the case of the white sifaka, males do indeed compete physically for females, and battles can become quite bloody. But for some reason this has not resulted in them physically dominating females, as Darwin would have predicted.  Perhaps due to Madagascar’s peculiar environment and the sifaka’s strange form of locomotion. A recent study revealed that when you live in the spindly dry forest, agility trumps brute force. If you’re being chased by a competitor and you are too big, you’re too slow and you’ll get caught. And if you’re too small, when you do get caught you won’t be able to fight. So, selection favors an intermediate body size and powerful long legs, explaining why competitive males have not evolved greater size and the female lemur retains her power and social dominance.

There are further evolutionary forces at play. Males have evolved a sneaky trick to monopolize their valuable egg without physical dominance or fighting one another: they have semen that hardens like rubber to form a ‘copulatory plug’. When females are only receptive for a short period, a male can temporarily enforce her chastity by clogging her vagina with his coagulated seminal fluids. These plugs can get pretty big. They don’t make it impossible for subsequent males to mate, but they need to be dislodged so they are a significant obstacle. When the female is only receptive for a day or even less, this might make all the difference.

Females, with their elevated reproductive costs, have higher nutritional demands than males and are more at risk from going hungry. Undernourished females are unlikely to produce quality eggs or support pregnancy and lactation, but a skinny male can still shoot viable sperm and fire his genes into the next generation. So, females have more to lose in the reproductive fitness stakes and will therefore be expected to fight harder for resources. Physical fighting is also costly and so it pays for males to defer to females and search out more food elsewhere rather than enter into an extended battle that they’re unlikely to win and that could instead cause significant harm. Given that most lemurs are the same size, and food is so scarce on this harsh and highly seasonal island, this could explain why those male sifaka repeatedly give up their precious baobab fruits after a couple of cuffs to the head.

Just like the spotted hyena, pregnant ring-tailed lemurs reveal elevated levels of testosterone along with the lesser known androgen androstenedione, in ring-tailed lemurs the levels of these during pregnancy can even predict the dominance of her resulting daughters.

It would seem that soaking in a prenatal androgen soup wires these fetal females towards aggression, giving them the competitive edge as adults. But if evolution is all about maximizing genetic success then this belligerent advantage is something of a double-edged sword. For the spotted hyena, increased aggression may help her and her cubs fight off rivals when feeding is highly competitive at a communal carcass. But the price is giving birth through a clitoris, which is not without its challenges. For first-time mothers it’s the eye-watering equivalent of squeezing a cantaloupe out of a hose pipe, which is why up to 60% of births are stillborn and 10% of new mums die in the process. There’s a long string of negative consequences to females being exposed to androgens who can experience difficulties with reproduction and mothering.

It’s a fine balance. Like the spotted hyena, ring-tailed females and their offspring may benefit from violently commandeering precious food sources in an otherwise barren Madagascan dry forest. But their aggression levels are so high that lemur mothers frequently end up brawling so hard with other females their infants end up dead.

A wide range of female mammals, from meerkats to the common garden mole, sport some degree of ‘masculinized’ genitalia. Most interesting is its presence throughout the prosimians – the group of primates that includes Madagascar’s lemurs, along with Asia’s lorises and Africa’s bush babies. All these primates come from the most primitive primate line that diverged from New and Old World monkeys some 74 million years ago. This suggests that androgen-mediated female dominance could have been the ancestral state of both lemurs and primates, including us.  This revolutionary proposition destroys the assumption that aggressive patriarchy is the universal nature of all primates.

SISTERS UNITE!.

Power in animal societies has traditionally been defined in terms of dominance through physical intimidation – which is a very male way of looking at it.  But there are other ways of categorizing power structures. Power can come from physical dominance or specialist knowledge of where to find the best fruiting trees, controlling access to unfertilized eggs, or strategic alliances.

When females are placed together in zoos, they generally decide rank quickly and with little fuss: one female will show her submission to another and that’s it. Female hierarchies are stable and rarely contested, maintained by respect from below rather than intimidation and strength from above, perhaps are better described as subordination hierarchies.

With male chimps it’s a very different story. Rank is determined partly by physical strength but crucially by tactical coalitions with other males. Alpha male status is frequently challenged and highly unstable. Power struggles generally involve complex and shifting alliances like human political maneuvering. In rhesus macaques and vervet monkeys, for example, a male’s quest to achieve and maintain dominance is strongly influenced by the support of high-ranking females.

Female vervet monkeys remain in their birth group and form strong lifelong bonds with their kin, while males disperse and join other, unrelated groups. This gives the females a huge amount of power. Matrilines of related females form the stable core and cooperate against male domination. Females will prevent certain males from joining the group and drive other males out, occasionally wounding or even killing them in the process.

As the stable nucleus of the group, females are often its brains; the keepers of essential environmental knowledge about where the best spots for sustenance or a safe sleep can be found. Female mammals often live longer than males, enhancing their expertise. Amongst capuchin monkeys, for example, it is the diminutive females that more commonly display leadership when it comes to foraging and group movements not the alpha male, challenging the age-old assumption that dominance and leadership are one and the same.

The more female matrilines are studied, the more group authority they command, influencing societal outcomes in ways that have traditionally been underappreciated when viewed through the prism of physical dominance, and thus chipping away at the assumed autonomy of the alpha male.

Unlike female vervet monkeys, once a female chimp reaches puberty, she leaves her birth troop and surrenders to a nomadic life, foraging alone in the forest. Any females she meets along the way will be viewed as competitors, so they don’t bond. If she happens to join a group, there will be no familiar family members to connect with and her only significant connection will be with her offspring. In contrast, males do not disperse and spend their lives surrounded by their family. Male chimps form the core of the troop, and over the course of their lives they develop complex relationships and supreme social muscle.

Dispersal patterns, then, can be a neat way of predicting the dynamics of power in social primates. The sex that stays in their birth group to always develop the strongest mutual bonds.

In addition to chimps, non-bonded female primates include gorillas, colobus monkeys and hamadryas baboons – whose females are the least emancipated of the bunch, with the dubious honor of being dubbed ‘the most wretched and least independent of any non-human primate’ by the anthropologist Sarah Blaffer Hrdy.

You do not want to be reincarnated as a hamadryas female. These social Old World monkeys live in large herds and scratch out a meagre life foraging for seeds and shoots in the semi-desert badlands of Somalia, Sudan and Ethiopia. Sexual dimorphism is extreme: burly males are twice the size of females, sport horrifying canines and a splendid white mane.

Virile males amass and maintain a harem of around 10 to 20 females in a uniquely creepy way, by kidnapping them from their families as pre-pubescent juveniles. From day one, the immature female is conditioned by her captor to unfaltering obedience by routine domestic violence. If she strays even a few meters for an impromptu sip of water, she will be hounded and attacked by her subjugator, occasionally with such force she’s lifted clean off the ground. These ‘excessively paternalistic’ males rarely cause grave harm to their hostages, however. Their hostility is carefully tuned to intimidate and control, without inflicting irreparable damage to their precious reproductive investment.

The communities in which women have least control over their lives, and are at most risk of male violence, are ones in which they are separated from their kin at an early age and have little support.

BONOBOS – A GIFT TO THE FEMINIST MOVEMENT — Frans de Waal

Where chimps are patriarchal and warlike, bonobos are matriarchal and peaceful. On arrival in another community, a young bonobo female will single out one or two senior resident females for special attention, using frequent G-G rubbing and grooming to establish a relation. If the residents reciprocate, close associations are set up, and the younger female gradually becomes accepted into the group – then, after finding a mate and producing her first offspring, the young female’s position becomes more stable and central.

Loretta controls the food amongst the bonobos in the San Diego Zoo. Access is often provided in exchange for sex. Both males and females will trade sex for food and, as a result, happily sit and feed together. This is in sharp contrast to chimps, in which males eat first with females sitting at a safe distance until they are fully sated. Unrelated females do indeed form long-term stable relationships with one another, facilitated by grooming and sex, and backing each other up and forming coalitions. Unlike male chimps, they don’t use their coalitions to fight one another but to overpower aggressive males.

Parish noticed that females were inflicting serious blood-drawing injuries on males – deep gashes, fingers and toes bitten off and she even witnessed punctured testicles. Frans de Waal, her supervisor, sent her a list of 25 injury cases that he had recorded whilst studying the bonobos in San Diego. Almost all were female-on-male attacks. Parish cast the net wider and discovered shocking tales from zoos all around the world.

‘It’s really clear that the females are not messing around. It’s serious and it’s dangerous for the males and they have a lot of fear of females,’ Parish told me. Male bonobos are very close to their mothers, whose rank and authority offer their sons protection against bullying by other females. In the wild, males will likely have their mother close by in their social group. So, whilst the threat of female aggression is very real, bonobos are actually much more peaceable than their chimpanzee cousins.

Chimpanzees are famously territorial. When neighboring 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. Very soon it looks more like a picnic than warfare.

The bonobo’s sex life is as creative as it is unrestrained. Males, for example, will enjoy each other’s company by ‘penis-fencing’, which sees them rubbing their ‘swords’ together whilst dangling from a branch. For females, the most frequent and preferred sexual activity is G-G, which they will choose over sex with a male if both present themselves at the same time.

There’s no bonobo that’s exclusively heterosexual or homosexual. They’re all bisexual.

Like humans, bonobos have a partial separation between sex and reproduction, with females frequently initiating and engaging in sex outside of their fertile period. But with the average copulation lasting 13 seconds, bonobo sex is fast, frequent, and as casual as a handshake.

Bonobos stare deeply into each other’s eyes, passionately kiss using tongues, practice oral sex and even fashion sex toys. Frances White, a biological anthropologist at the University of Oregon, once watched a female bonobo turn a stick into a kind of knobbly French tickler, which she then proceeded to take great pleasure in.

When bonobos do have heterosexual sex, they often do so in the missionary position. This is not really seen in any other primates. Chimpanzees virtually never have sex face to face, whereas bonobos do so in one of three copulations in the wild.

The first suggestion that the sexual behavior of bonobos in some ways mirrored our own arrived way back in the 1950s, but the scientists involved chose to obscure their controversial findings by reporting in Latin. Eduard Tratz and Heinz Heck reported in 1954 that the chimpanzees at Hellabrunn Zoo mated more canum (like dogs) and bonobos more hominum (like people). In those days, face-to-face copulation was considered uniquely human, a cultural innovation that needed to be taught to preliterate people (hence the term ‘missionary position’). These early studies were studiously ignored by the international scientific establishment. It wasn’t until the sexual liberation of the 1970s that the full glory of the bonobos’ sex life started to go public.

HOW DID WOMEN BECOME SO UNEQUAL IN HOMO SAPIENS?

Barbara Smuts points to our ancestors’ gradual switch from hunter-gathering to intensive agriculture and animal husbandry. While cooperation on hunts gave men the possibility of controlling food resources, women’s contribution to foraging limited this control. The smaller plots of land associated with the switch to intensive agriculture and animal husbandry, however, limited women’s movement and gave males control over resources and an incentive to form political alliances with other males, to fight rival males and control females.

A foraging lifestyle makes it much harder for males to restrict females’ movements and access to resources, as they are able to get their own food and other resources. But once females were restricted in their activities and males gained control of high-quality foodstuffs, like meat, females lost agency and became sexual property. Paternity became an issue, as property was inherited, and patriarchy took hold. The evolution of the capacity for language allowed males to consolidate and increase their control over females because it enabled the creation and propagation of ideologies of male dominance/female subordinance and male supremacy/female inferiority.

But it doesn’t have to be this way. Their story shows us that males are not genetically programmed to aggressively dominate females. Across species, their ability to do so depends on environmental and social factors. The key ingredient for female empowerment is the strength of the sisterhood, from family to friends, to overthrow an oppressive patriarchy and foster a more egalitarian society.

We have a lot to learn from bonobo females. The feminist movement argues that if you behave with unrelated females as if they are your sisters, you can gain power. The bonobos show us that that’s true. It gives us a lot of hope.

Academia is a hotbed of competition and ego, with researchers jockeying for their animal and research to be the most relevant. If you’ve built a career around proving that humanity’s patriarchal roots pass through chimpanzee culture and beyond, it’s not easy to write off a lifetime of data and start afresh. ‘I think it came as a shock, as it was so contrary to what we think is “natural” in the world,’ Parish told me. ‘There was a lot of sexism in people’s reactions. Some of my male colleagues didn’t want to recognize bonobo society as female dominant.’

Frans de Waal agrees with Parish – the primatologists who want to marginalize the bonobos are never women. ‘It’s all men,’ he told me.

Most agree that in captivity female bonobos are always dominant over males. In the wild, de Waal explained, the hierarchy is more mixed, but the top spot is usually a female or two, then perhaps a male. Most males are subordinate to most females.

Killer Whales

Killer whales are the most pumped-up member of the dolphin family and, like their smaller squeaky cousins, they’re highly social creatures with the smarts to match. Their whopping seven-kilo brain has more surface area for complex thought processes like language, social cognition and sensory perception than any other animal on the planet.

No other mammal known to science maintains lifetime contact between mothers and offspring of both sexes. There is always a bias towards dispersal of one sex, and typically, in social mammals, it’s the sons that leave. Some of these orca matrilines contained up to four generations of male and female orcas. Could this unique structure have something to do with the female’s exceptional post-reproductive lifespan?

Aside from humans, killer whales are the most widely distributed predators on the planet. Highly specialized hunting skills have enabled these cosmopolitan killers to exploit particular prey types from the Arctic to the Antarctic. For example, orcas off the coast of New Zealand specialize in digging up and devouring stingrays. In Argentina, they surf on to shore to snatch sea lion pups from the beach. Along Alaska’s Unimak Pass, they gather in May to ambush young grey whales, and in Antarctica they use synchronized swimming to generate waves that wash seals from the safety of the ice floe – and into their mouths.

These particular orca races are known to ecologists as eco-species, as they’re the same species but inhabit a specific geography and do not interbreed. More than that, they are known to ‘speak’ their own dialects and their specialist hunting techniques, passed down from generation to generation, have been compared to culture.

Despite the tough name, male killer whales are, according to whale experts, ‘massive mummy’s boys’. They spend most of their lives swimming a few feet from mum’s side but, significantly, her hunting handouts help keep them alive.  If a male orca’s mother died before his 30^th birthday, he was three times more likely to die the next year. If she passed away after he turned 30, he was 8 times more likely to die the following year. But if mum had gone through menopause, his odds of dying the next year went up by 14 times. The data was irrefutable: sons whose mothers live a long time after giving birth to them have a survival advantage over those whose mothers die earlier, and that only becomes truer as both mother and son age.

There’s still a problem with this theory: it doesn’t explain why females would stop reproducing halfway through life. Old female elephants are repositories of ecological and social knowledge, but they don’t have a menopause. They are the chiefs of their family group, carrying the wisdom to outwit lions, form political alliances with other female elephants, and remember ancient water sources during times of drought. These charismatic giants have much in common with killer whales (and indeed humans) – long lives, big brains, complex communication skills and a large, fluid social network. Not only were the older matriarchs more likely to tell friend from foe, they could also distinguish between the roars of a male and a female lion. This is a vital skill because although they sound almost identical, their threat is anything but. Whereas female lions are normally the primary hunters, when it comes to snatching elephant calves only males, who are 50% bigger, can afford to take on such sizeable prey. The older matriarch’s superior powers of discrimination keep her clan safe, relaxed and focused on that old priority: eating. Research shows that the quick-thinking and confident leadership of older matriarchs’ results in an increase in offspring, supporting the grandmother hypothesis.

Having kids is expensive, but with orcas there is an interesting disparity between the cost of sons and daughters. When a young female orca starts reproducing, around the age of 15, she needs 40% more salmon in order to produce the rich milk required to suckle her calf. Therefore, when a ‘daughter’ reaches maturity she suddenly places a significant toll on the nutritional demands of the pod. Sons are a different story. When pods mingle they will mate with females outside their matriline, and although they may remain surprisingly close to their mother even when having sex, their offspring will be brought up by the mother in that different matrilineal pod. So for a mother, feeding her son’s genetic legacy comes at the expense of another matriarchal group, which is far cheaper than if she has a daughter.

Evolutionary theory predicts therefore that mothers will indulge their sons far more than their mature daughters, and this was indeed demonstrated by a 12-year study on food sharing in killer whales. Conversely, it also predicts conflict between mothers and their female progeny once the latter reach sexual maturity, as a result of some unique kinship dynamics. When a female orca is born, her father is in another pod and so her relatedness to the males in her own pod is low. As she ages, her relative relatedness to the pod increases as she produces sons and grandsons. Mothers are therefore always more related to their pod than their daughters and granddaughters are. This asymmetry of relatedness promotes conflict between female generations breeding at the same time.

Natural selection will favor young mothers, who have less stake in the success of the wider group, who aggressively compete for limited resources. This prediction was borne out by the observation that when orca mothers and daughters bred simultaneously, calves born to older mothers were almost twice as likely to die in the first 15 years of life as those born to the younger mothers. This social cost to late motherhood provides the evolutionary impetus for a female orca to stop breeding mid-life so she can invest in her sons and grandsons and stop competing with her daughters and granddaughters.

That incentive doesn’t exist in elephants because their sons, like most social mammals, eventually leave their birth group. So elephant females become less related to their group-mates over time or, at least, no more related. An elephant matriarch’s best bet, then, is to carry on reproducing until she dies.

Orca brains are the heaviest on the planet – around 7 kilos – and huge. Humans have an EQ of around 7.4–7.8 and chimpanzees of around 2.2–2.5. Female orcas have an EQ of around 2.7, which is higher than a chimpanzee’s. Orcas have evolved proportionally more of the thinking part of the brain than humans have. Their cerebrum makes up 81.5% of brain volume compared to our 72.6%.  Orcas also possess an enigmatic extra lobe of tissue that’s snuggled in between their massively elaborate neocortex and the limbic system where emotions are processed.

This so-called paralimbic lobe is only found in dolphins and whales. It provides dense connections between the two neighboring areas of the brain and suggests that orcas could be processing emotions in a way we cannot comprehend, with dimensions to their emotional rainbow we don’t have. Orcas have other parts of their brain involved in social awareness and communication that are also unusually complex. So many parts of their cerebrum that are more elaborate than primate brains, and these are the parts that do social cognition, awareness, problem solving, perhaps making them quite emotionally sophisticated, lightning-quick thinkers with many more dimensions to their communication than we have.  Perhaps these ‘socially complex brainiacs’ might even have a distributed sense of self that’s bound to the group, as well as the individual. This could explain the extraordinary levels of social cohesion that occur, even to their detriment. For example, the reason the southern residents were so massively plundered by marine parks is that when one animal was caught, its family would remain by its side and could be added to the catch with tragic ease.  Leaving the group was unthinkable for them.

‘They’ve got a whole ocean to swim in and yet they’re swimming not just next to each other but touching each other. The family group is their home, they safe space, the key to survival.  So it pays for orcas to stay close and connected, in ways we cannot comprehend.

They certainly display extraordinary levels of social support, including babysitting for each other’s calves and caring for disabled individuals. Giles told me of a male orca from a transient mammal-eating pod, outside of the southern residents, that has scoliosis, yet is a thriving member of his family. ‘They bring him food,’ she told me. ‘It’s hard for him to keep up with them, but they loop back and bring him chunks of whatever they’ve killed. In a lot of human cultures they’d leave such an individual behind.

Not all orca females make great leaders, though since they have different personalities. The relationship between personality and leadership has been more conclusively probed in the Amboseli elephants, where behaviors are somewhat easier to observe than in a fast-moving submarine mammal, where personality differences play a major role with elephant matriarchs, although it’s hard to quantify as families tend to perpetuate certain traits down their ancestral line, traits like confidence, curiosity, or nervousness. Leading the clan was less about being dominant and exerting power – less than for, say, an alpha male chimpanzee – and more about elevated levels of influence, knowledge and perception that earned the respect of the other elephants.

Elephants, like orcas (and great apes, like us), have what’s called a fission–fusion society, meaning their social lives are fluid. Group size isn’t fixed, it is dynamic and can change by the hour as members split off and then rejoin one another. They’re not told where to go, but this leadership is an attractive social center. The matriarch is the glue that holds everyone together. Losing this wild old female focal point shatters their social world as the clan are robbed of their library of ecological and social knowledge – the very thing they need to help them out of tough times.

The social impact of bereavement is enormous. Grieving animals are not as responsive to others. So that has a knock-on effect on how closely they’re bonded; they’re a bit depressed, they don’t spend as much time feeding and they don’t tend to group needs, which leads to a higher proportion of family fission immediately after matriarch loss. In one group, the next oldest female was 44 and could have taken charge but ‘she couldn’t be bothered with everyone else and left. The next oldest was a bit of a flake, so the youngest female, just 27 years old took the top job.

LIVING WITHOUT MALES: CLONING AND PARTHENOGENESIS

The mourning gecko is a one-lady lizard-making machine, capable of creating up to 300 clones of herself during her short five-year life. This shouldn’t, of course, be possible. The mourning gecko has somehow evolved to cheat this fundamental process. She joins a very exclusive female-only club of around one hundred known vertebrates – an assortment of fish, lizards and amphibians – and a host of spineless wonders only really visible to microscope owners, but whose sex lives (or lack thereof) are exploding evolutionary paradigms left, right and center.

Their remarkable asexual skill is known as parthenogenesis, from the Greek meaning ‘virgin’ and ‘birth’. It has enabled the mourning gecko to colonize not just the Hawaiian Islands but Sri Lanka, India, Japan, Malaysia, Papua New Guinea, Fiji, Australia, Mexico, Brazil, Colombia, Chile and many, many more places.

The problem with cloning is all offspring are genetically identical to their mother. Essentially, it’s the ultimate form of inbreeding – there is no way to create genetic diversity, except for the occasional copying mistake during meiosis. So, animals that clone themselves leave their lineages vulnerable to parasites, disease and environmental fluctuations, which they lack the genetic variety to counter.

The four thousand or so species aphids, a small sap-drinking insect are despised for sucking the life out of crops and spreading disease. They are also, quite possibly, the virtuosos of the cloning world. At the start of summer, a single female will give birth to 50–100 whole females, each already pregnant with embryos developing inside her. Like little plump green Russian nesting dolls this telescoping of generations shortens the nymphs’ maturing time to just ten days and enables aphids to boom exponentially. Some species of cabbage aphid can produce up to 41 generations in a single season. Just one female hatched at the start of summer could theoretically produce hundreds of billions of descendants, were it not for ladybirds gobbling them up.

In the autumn, once the damage is done and their numbers are legion, the females reproduce sexually with male aphids, and lay down eggs with the necessary genetic variety to cope with whatever the following year throws at them. It’s a bulletproof system that’s turned them into the gardener’s greatest nemesis. In the end, the aphid always wins.

You may feel that you’ve weathered some overly long sexual droughts, but they are nothing compared to the bdelloid rotifer, whose commitment to celibacy is unmatched in the animal kingdom. These microscopic relatives of the flatworm haven’t had so much as a sniff of sex for some 80 million years. All 450 species of this class of rotifer are female. Some scientists think that the bdelloids can extract DNA from their dinner and spruce up their own genome by a process called ‘horizontal gene transfer’. Studies have shown that up to 10% of the active genes in these rotifers could be pirated from other species. The bdelloids appear to have adopted a Frankenstein collage of foreign DNA from more than 500 different species. Whether that’s through ingestion or not is up for debate, but these pilfered genes provide the bdelloids with much-needed genetic variation in the absence of sex. In nature’s edition of the TV reality show Survivor, the bdelloid rotifers would probably be the last animals standing. They can survive several years of desiccation and high blasts of radiation. As far as we know, they are the most radiation resistant creature on the planet, beating even the famously indestructible tardigrade in the hard-nut stakes. The bdelloids are able to survive and produce viable replicas of themselves because their mosaic of stolen genes code for enzymes that give them the remarkable ability to repair their shredded DNA.

One study took several species of whiptail – both asexual and sexual – and housed them in an enclosure for close observation. The all-female species behaved very differently to their sexual cousins. Same-sex couples were much more likely to shack up and share burrows than their sexual relatives, who tended to sleep alone at night. The sexual societies also showed four times more aggression against one another than the asexual species. Sexual species got into more fights, did more chasing as they tried to steal one another’s food and had a stronger dominance hierarchy.

The all-female clones share 100% of their DNA with each other, making them significantly more closely related to one another than the sexual whiptails. This kinship could account for their increased cooperation. Leuck observed that males were the instigators of much of the aggression, suggesting that, in whiptails at least, an absence of males results in a more tolerant society.

The success of these all-female species demonstrates a new dimension in the battle of the sexes, with males fighting not just to fertilize eggs, but to simply exist. All-female societies are twice as productive without the dead weight of males, whose offering of genetic diversity is now understood to be less crucial than previously assumed. Recent mathematical models have revealed that evolution need not favor sexual reproduction, even when it does increase variability that is beneficial, and so, the question of sex remains an enigma.

In recent years, virgin births have been cropping up in all sorts of unexpected species and places – for instance, sharks in Nebraska. This land-locked Republican Midwestern state isn’t exactly known for its ocean life, miracles or indeed female emancipation. But a species of hammerhead shark changed all that when she gave birth in a zoo aquarium in Omaha, surprising everyone. Her tank-mates were two other female hammerhead sharks and an assortment of rays, so who (or indeed where) was the daddy? Female sharks have the ability to store sperm for months, if not years, so it was assumed this shark, let’s call her Mary, must have mated prior to being taken captive. The aquarium soap saga continued when the pup was killed by a stingray after just a few days of life. The unfortunate tragedy did at least give researchers the opportunity to do genetic analysis, which proved there was no ‘DNA of male origin’ in the baby shark. Gifting local papers with a unique opportunity to compare a man-sized shark with the mother of Jesus.

The shark discovery proved to be another paradigm shifter. Parthenogenesis was otherwise unknown amongst the cartilaginous fishes, the primitive group to which sharks belong. They now join the bony fish, amphibians, reptiles and birds on the asexual bandwagon.

With environments becoming increasingly fractured and with so many species in catastrophic decline, finding a viable sexual partner is likely to become increasingly hard. Females that can fall back on the ancient art of cloning might just be what’s needed to help species weather tough times.

The sawfish, a type of ray with what looks like a chainsaw attached to its face, has recently been documented doing just this. Native to the rivers of west Florida, it is one of the world’s strangest, and most critically endangered, sharks – sawfish numbers have declined to 1–5% of their original population size. In 2015 researchers at Stony Brook University analyzed telltale markers called microsatellites in 190 sawfish that reveal how related their parents are. In seven fish, the markers suggested their parents were identical to them. Which can mean only one thing: female sawfish had started to clone themselves. This is the first ever documentation of this type of parthenogenesis in a shark, or indeed any kind of vertebrate, in the wild. It signals something horrifying – a tragic tipping point for a species on the cusp of extinction. But the discovery of these pioneering parthenogenetic females also provides me with a chink of hope.

There is no known example of a mammal having a virgin birth, either in captivity or the wild. Fundamental aspects of mammal biology make it unlikely we ever will find any mammal self-replicating in nature. So, it looks like men can sleep safe (for the time being).  Which, as we are the architects of all this destruction and the ultimate ‘weed’ species, is for the best. The idea of humans reproducing like aphids is a truly terrifying scenario – and most certainly not what this planet needs right now.

Homosexual and other kinds of sex

Darwin documented his salty gifts with a zeal few had shown for barnacles before, or indeed since. This labor of love proved so all-consuming it delayed the publication of Darwin’s book on the origin of species by many years while he painstakingly produced four exhaustive volumes on the world’s barnacles, both extant and extinct. The barnacle’s sedentary life is a boon for personal safety, but less so for sex: locating a mate isn’t exactly easy when you’re glued to a rock. Darwin discovered the barnacle’s secret weapon is an extravagant penis, the longest relative to body size in the animal kingdom. It enables the barnacle to cruise the neighborhood for sex, whilst remaining cemented to the spot head first.

Every individual has both male and female reproductive organs so they can fertilize and be fertilized by all of their neighbors. And if there’s no one else within reach, as a last resort the barnacle can recall their roving inseminator and fertilize themselves.

In 1848 Darwin stumbled upon a specimen with no penis at all. Not only that, it appeared to be infested with tiny parasites. Darwin had been picking them off and throwing them away when he realized his mistake. The barnacle in question was a female and the microscopic ‘parasites’ were the male of the species, albeit somewhat abridged: mouthless, stomachless and short-lived.

A century and a half later, state-of-the-art research using DNA markers has confirmed that Darwin was indeed right. Barnacles display a rich diversity of sexual systems – from hermaphrodite to separate sexes to a mixture of both – allowing scientists an exceptional opportunity to study evolution in motion.

Darwin’s sexual selection theory considers the only role of sex to be procreation. Through this lens homosexual activity is denigrated to an inconvenient ‘error’ and subsequently ignored. Building on the work of the Canadian biologist Bruce Bagemihl, whose landmark modern bestiary catalogued homosexual activity in over 300 species of vertebrate, Roughgarden extolled the role of same-sex activity in fostering cooperation amongst animal societies. We’ve seen this social glue at work with the bonobos.

Roughgarden includes numerous other species, from a wide range of taxa, where homosexual activity has, in her opinion, evolved as ‘a social-inclusionary trait’. These include a long-term study in the Netherlands where European oystercatchers, the monochrome marine birds common to many coastlines, have been documented nesting in ‘threesomes’ featuring two females and a male. These family units can be either aggressive or harmonious, depending on whether the females in the group are having sex with one another or not.

Such breeding strategies are generally branded as ‘alternative’ for betraying the nuclear family ideal widely assumed to be nature’s norm. Roughgarden queries this pejorative label and argues how countless animal families frequently fail to conform to this ‘Noah’s Ark view’. In some species males and females have multiple sexual forms and identities, which she argues should be considered as different genders.

If you go snorkeling on a reef, chances are a quarter of the fish you’ll see are serial sex changers. The bluehead wrasse is just one of many rainbow-colored reef fish that undergo a natural sex change during their adult life. Known as sequential hermaphrodites, these fish begin life as one sex and are triggered to switch camps by a social stimulus, such as the loss of a dominant individual or the relative availability of the opposite sex. For some, like the flamboyant parrotfish, the change is permanent – once they’ve made the switch they’re stuck as that sex until they die.

Others have a more flexible sexuality and can switch back and forth throughout their life. This is a handy trick if, like the coral goby, you live in a crevice and are not that keen on venturing out much for fear of being eaten. If another coral goby comes along you can always reproduce, whatever its sex, by simply switching gonads to complement your new mate.

Some of these sex changers can flip with astonishing frequency. The chalk bass, a neon-blue Caribbean fish that’s about the size of your thumb, has been known to switch sex up to 20 times a day. Chalk bass don’t do this in order to play the field; quite the opposite – switching sex is their recipe for relationship success. Chalk bass are known to display unusual levels of sexual fidelity and are considered more or less monogamous. Their sex-change habits are a coordinated response with their long-term partner. Researchers believe that taking turns laying eggs, which are bigger and more energy-consuming to produce than sperm, keeps the reproductive investment fair. Each fish fertilizes as many eggs as it produces. Proving that even with fish you get what you give in a relationship.

Anemonefish (think Nemo in the Disney film) are monogamous reef dwellers who set up home together in an anemone, whose stinging tentacles offer the couple, and their eggs, protection. The belligerent female is the boss in the relationship – it’s her job to defend the territory while the male cares for the eggs. The fish live surprisingly long lives – up to 30 years – in the same anemone, often with a bunch of juvenile males in attendance. If the female is removed, say nabbed by a barracuda, it will trigger Mr Anemonefish to transform into the new dominant female, and one of the juvenile males to mature into her mate. A biologically accurate version of this hit movie would therefore have seen Nemo’s father, Marlin, transition into a female, and then start having sex with her son, which might have made for a less popular family film amongst Disney’s die-hard conservative audiences.

Rhodes’ research has shown that the male-to-female sex change starts first in the brain and it’s only later, after months or even years, that the fish’s gonads catch up and become fully female.

There are around 500 known species of hermaphrodite fish. Likely many more. It’s a nifty strategy to maximize your reproductive chances in the vastness of the ocean. Hermaphrodites are widely distributed across all taxonomic groups of fish, including the most ancient. The terrifying-looking hagfish is a muscular snake-like fish which, once seen, will haunt your nightmares. Also known as the slime eel, it has no scales, no spine and no jaw, but it does have whorls of sharp teeth for mincing the flesh of any decaying critters it sniffs out on the ocean floor using its solitary nostril. As a lonely bottom feeder ploughing its slimy trade in the bleakness of the ocean depths it can be hard to find love, and several species of hagfish are known to spread their sexual options by sporting both an ovary and a testis. The hagfish hasn’t changed for some 300 million years and is considered a primitive ancestor of modern fish, suggesting to Rhodes that hermaphroditism could be the ancestral state of not just fish, but all vertebrates.

Whether the issue is semantic or philosophical the fact remains that mainstream biology is proving slow to evolve beyond basic binary definitions of sex and recognize the facts of biology, which is somewhat ironic. ‘I’ve come to the conclusion that the human brain likes black-and-white examples. It likes things to be one thing or the other, but that’s problematic when it comes to sex,’ Crews offered as his explanation for this paradox. It is Crews’ belief that viewing the animal kingdom through binary goggles has forced scientists like Darwin, and many who followed in his footsteps, to focus on the differences between the sexes, when studying the parallels could be more revealing. ‘People forget that the majority of traits in males and females are similar. We all have brains, we all have hearts, we all have our bodies. There are more similarities between the sexes than there are differences.’

And individual variation within a sex is greater than the average variation between the sexes

Rather than thinking of the sexes as wholly different biological entities, we should consider them members of the same species, with fluid, complementary differences in certain biological and physiological processes associated with reproduction, but otherwise much the same.

Four years after the publication of The Descent of Man the American minister and self-taught scientist Antoinette Brown Blackwell published The Sexes Throughout Nature, in which she argued that Darwin had misinterpreted evolution by giving ‘undue prominence to such as have evolved in the male line’. The more complex or advanced the organism, she suggested, the greater the division of labor between the sexes. For every special character males evolved, females evolved complementary ones. The net effect being ‘organic equilibrium in physiological and psychological equivalence of the sexes’.

Blackwell was no lone voice. A handful of women intellectuals, all self-educated, read Darwin’s work and recognized that the female of the species had been marginalized and misunderstood. But these early feminist voices were ignored by the scientific patriarchy.

Thankfully, Hrdy’s voice, along with the other twentieth-century feminist scientists, was finally heard, albeit after much shouting. These women benefited from an egalitarian education and the associated intellectual confidence that enabled them to take on the second wave of scientific sexism, peddled by notorious neo-Darwinist male evolutionary biologists and psychologists. Their groundbreaking work has helped forge a radical shift in our understanding of not just what it means to be female, but of evolutionary theory itself.

I don’t really understand why the names of the most published and prolific of these revolutionary scholars – Hrdy as well as Patricia Gowaty, Jeanne Altmann and Mary Jane West-Eberhard, amongst others – are not more widely recognized for the scientific and cultural impact of their work. In my mind, they deserve to be as famous as their male counterparts – Robert Trivers, Richard Dawkins, Stephen Jay Gould et al. But for some reason, even though their ideas are now woven into modern evolutionary thinking, the female authors of these bold new perspectives are still relatively invisible.

On one of our many long phone calls, Gowaty, whose work has successfully exposed, and sought to replace, much of the bigotry that plagues evolutionary theory, expressed an almost tearful gratitude for my interest in her work, lamenting, ‘I’ll be famous after I am dead.’ I hope this book helps give these innovative thinkers the recognition they deserve.

A 2018 analysis found that images of males and females in evolution textbooks still reinforced stereotypical sex roles and ‘did not reflect the shift happening in the scientific community’

Bias lurks in language too. A recent study found that science authors still use active words to describe males, but passive words to describe females – males have ‘adaptations’ and females ‘counter-adaptations’. In other words, males act, whereas females react. Stereotypical labels – ‘caring’ females and ‘competitive’ males – are still bandied about in academic literature as if they were incontrovertible facts with no apparent need for back-up citations to justify their use.

Research is still directed towards males, whether intentionally or not. The ‘type specimens’ that define a species, and form the great library of life in the world’s natural history museums, are heavily biased towards males. When females are used, they aren’t necessarily representative either. The Harvard neuroscientist Catherine Dulac told me how the little white mice that form the basis of much laboratory research have been domesticated by chauvinism. In the wild female mice are just as aggressive as males – they attack unknown suitors and cannibalize babies. But their aggressive nature has been bred out over the years to create a model animal that represents ‘what a female should be’. This fake female then forms the model basis of much lab-based behavioral and neurobiological research.

Even when model organisms aren’t bred towards a patriarchal ideal, they can still uphold those norms. Model systems are meant to provide general results for a given aspect of biology, but the species chosen are often questionable. Their use is often trapped by history and convenience, rather than relevance. Fruit flies, for example, still dominate sexual selection research and account for almost a quarter of all the papers published on this subject. Yet they fell into that model role purely because their breeding cycle is compatible with the academic calendar. Thus helping scientists more than the science they practice. The fact that their sexual behavior is not representative of other insects, let alone taxa, hasn’t stopped their eccentric kinks being extrapolated as sexual role models for all animals, even us.

Marlene Zuk, professor of evolutionary biology at the University of Minnesota, has cautioned against the use of improper model systems and campaigned for diversity; both in terms of wild and captive specimens, but also the range of species used. She argues that if we were starting from first principles we would never have chosen fruit flies as the basis of sexual selection research, and that their quirks have helped fuel confirmation bias. She’s cautioned how ‘taxonomic chauvinism’ is a very real thing and means that certain animal groups – namely insects and birds – that are either charismatic or convenient, have dominated sexual selection research, ironing out natural diversity.

Researching this book was a liberating experience. I no longer feel like a sad misfit. Females are not destined to be passive and coy, evolutionary afterthoughts just waiting to be dominated by males. Even when we are physically weaker, we can still be powerful.