Bitch: On the Female of the Species

by Lucy Cooke

West-Eberhard did not attempt to discredit Darwin, but instead proposed expanding his principles so that sexual selection became a subset of the broader backdrop of social selection. She illustrated her argument, much like Darwin himself did, with a vast array of creatures whose flamboyant traits or sexual dimorphisms could not be explained by sexual selection alone, and might even have different social functions depending on the time of year and situation.

She outlined how dung beetles’ horns, pheasants’ tails, toucans’ beaks, birds’ songs and the dominance behaviour of bees and wasps could all be explained by the broader category of social, if not sexual, selection.

Many zoologists don’t see the need to invite yet another form of selection to the evolutionary party. Let alone one proposed by someone other tha...

Darwin’s definition of sexual selection isn’t expansive enough to explain elaborate traits like birdsong or indeed bright plumage and ornamentation in female birds. Worse still, Darwin’s narrow focus has ‘clouded our view’ and fostered a scientific bias that assumes such elaborate traits and sexual dimorphisms must all be to do with mating success, when they’re often to do with other forms of social competition.

it is becoming clear that females are just as competitive as males; it’s just the focus of their efforts is often different. While males clash primarily over access to females, females are more likely to fight over resources related to fecundity and parenting. And while their efforts may be more surreptitious, female competition is just as influential in shaping the path of evolution as male fighting – perhaps even more.

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.

‘Females are not innately disposed to organize into hierarchies… primate males appear to be the archetypal “political animal”,’ was the woeful conclusion of Female Hierarchies, the first ever textbook specifically devoted to female dominance relations. This could not be more wrong. Strategic competition amongst females is central to primate organization. Most female primate societies feature stable heritable matrilines, which compete with one another using psychological intimidation, tactical alliances and cruel punishment in their ruthless battle for control.

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

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.

As the biggest and most violent meerkat in the mob, she’ll use extortion, physical abuse, entrapment and murder to achieve this end.

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.

‘You regularly see dominant meerkats evicting their older daughters. They are brutal: if their daughters don’t get the hell out, they kill them.

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. This they do in the safety of their very own royal chamber aided and abetted by supporting castes of sterile workers and soldiers.

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 centimetres 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 twenty thousand 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.

The rest of the several million termites in the colony, other than the king, are rendered sterile and kept in their lowly castes by ingesting pheromones secreted by the royal anus, all of which makes the British monarchy suddenly seem quite reasonable.

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

Faulkes has spent the last thirty years investigating the naked mole rat’s eusocial society. 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, although she can squeeze out many more – an eye-watering twenty-seven was recorded in one litter.

Like a social insect queen she also lives ten times longer than the workers of the colony, but with no age-related decline in her fertility, thereby allowing her to leave an extraordinary genetic legacy during her abnormally long reproductive life. One legendary queen reared more than nine hundred pups during twenty-four documented years.

‘“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. Because they’re competing for the throne and they’ll kill anyone or die in the process. It’s super brutal,’ Faulkes said. These professional burrowers have evolved a ferocious bite. A quarter of their entire body musculature is devoted to powering their jaws to crunch through baked earth – and then there’s those javelin teeth. When females turn these industrial excavation tools into weapons things get ugly

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. They are an incredible advert for the power of cooperation, but also reproductive despotism.

As Faulkes said, ‘Naked mole rats are a brilliant example of a sort of utopian, almost communist society, but of course, lurking under that, there’s all kinds of sinister shit going on.’

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.

in 90 per cent of the 111 species it is the females who call the shots sexually, socially and politically. Madagascar is an island of bossy bitches – a land where female primates rule. This tale of female empowerment provides sharp contrast to the familiar patriarchal narrative of primate life, featuring a despotic male chimp beating his chest and terrorizing society with brute force – a popular social model for our own ancestry.

Lewis studies white sifaka, Propithecus verreauxi, which just happened to be in my top ten of must-see species. Long before I knew they were female-dominated I wanted to meet these strange bug-eyed, snow-white prosimians because of the way they move: sifaka don’t walk, they dance.

For while Fossey and Goodall were describing dominant silverback gorillas and the hierarchies of male chimpanzees on mainland Africa, Jolly was in Madagascar, quietly documenting something completely different – antagonistic alpha females. Jolly arrived in Madagascar in 1962, aged twenty-five, with a brand new PhD from Yale and a big juicy ‘Sputnik-era research grant to swell my pride’. She established herself at Berenty, in the isolated south, and set to work documenting the island’s peculiar and poorly understood primate life. Her chief obsession was the absurdly charismatic and now justifiably famous ring-tailed lemur, Lemur catta.

For a start, it is the females that do the majority of territorial defence. 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 probably linked to competition with other females, while males don’t pose much of a threat to them and can safely be ignored.

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.

In Madagascar I watched male ring-tailed lemurs subjected to routine physical harassment – biting, shoving and hitting – to surrender their food, a cosy sleep spot or prime patch of sun. Like the sifakas, these stripy lemurs take their sunbathing very seriously – legs akimbo, arms outstretched and eyes rolling back in ecstasy as they soak up rays with the unashamed enthusiasm of a Brit in 1970s Benidorm.

Jolly described an incident where a female intervened to stop a juvenile being bullied by an adult male, and ‘put him in his place’, and concluded that ring-tailed lemurs are the only wild primates ‘where all females can be said to be dominant over all males’.

Jolly also dared to suggest that her badass female lemurs might also provide ‘a particularly exciting glimpse of our history’. Madagascar’s lemurs are prosimians – our most basic primate cousins. They evolved from an early offshoot of the main primate evolutionary path that subsequently went on to divide into the New World monkeys (simians that inhabit the Americas) and Old World monkeys (simians of Africa and Asia, which led to the evolution of all great apes, including us).

This pioneering group of ancestral primates then evolved in isolation on this vast and relatively unpopulated island, radiating into a remarkable diversity of species from the tiny mouse lemur, Microcebus berthae, weighing no more than thirty paperclips (it is the world’s smallest primate), to one the size of a silverback gorilla, Archaeoindris fontoynontii (now sadly extinct).

Her discovery of this early branch of fierce, frightening females eroded the idea that aggressive male patriarchy is the natural state of affairs for all primates. Or, at least, it should have. Jolly’s groundbreaking discovery fell on deaf ears. Even her most studious revelations failed to undermine the prevailing idea that ‘order within most primate groups is maintained by a hierarchy, which depends ultimately primarily on the power of males’. In the sixties and seventies primatology was well and truly hypnotized by showy male dominance systems.This obsession began way back when the science emerged in the 1920s.

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, just as it was gaining momentum. Baboons, genus Papio, became the go-to model because they live in large social, semi-terrestrial troops on savannahs, similar to the environment scientists believed our ancestors inhabited.

Later, in the late seventies, chimpanzees took over as the model for human ancestry. Jane Goodall’s revelations of their warlike nature fuelled 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 antagonistic.

This enthralment with a handful of terrestrial, Old World species as models for human evolution resulted in what the anthropologist Karen Strier has dubbed ‘the myth of the “typical” primate’. These idiosyncratic macho monkey societies became the perceived blueprint for all primates. Subsequent phylogenetic research has, however, revealed that Old World monkeys make for poor primate prototypes. Their behaviour is actually highly derived, tailored to meet specific environmental challenges and far from representative.

But this natural diversity was overlooked – not just the lemurs but also the New World monkeys.

The reluctance to recognize female dominance saw it swept aside as strategic male ‘chivalry’ or demoted to simply female ‘feeding priority’. According to Lewis, the study of female dominance remains ‘intellectually isolated’, often dismissed as ‘a weird quirk of Madagascar’ – the ultimate untestable hypothesis. But given that 10 per cent of lemurs are not female dominant, this decidedly unscientific argument doesn’t hold a lot of water. It also ignores the global range of mammals, from carnivores to rodents and hyraxes, that have also been described as female-dominant, suggesting it can’t just be a Madagascan phenomenon.

So 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,’ Lewis told me. Lemurs have an especially short breeding season – in white sifaka it’s just thirty minutes to ninety-six hours a year, and in ring-tailed lemurs four to twenty-four hours.

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. Lewis thinks this could be to do with Madagascar’s peculiar environment and the sifaka’s strange form of locomotion.

So, selection favours 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. Just as we saw with the genitals of ducks, sexual conflict is also involved. Lemur females are promiscuous but 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’.

Amy Dunham, associate professor of ecology and evolutionary biology at Rice University, found that copulatory plugs are more common in species with short fertile windows (like the lemurs) and no difference in size between the sexes. She believes this alternative form of mate guarding offers an additional explanation for why male lemurs didn’t evolve to physically dominate females with increased size and weaponry.

Female lemurs are also wired for aggressive competition. Christine Drea, the Duke professor we met in chapter one studying the spotted hyena, has noted that many lemurs also share the same giveaway physical quirk: ‘masculinized’ genitalia. The spotted hyena (Crocuta crocuta) is a candidate for most domineering female mammal on the planet.

Some lemur species have a pseudo-scrotum with ‘skin identical in composition to that of the male’s scrotum’ and many boast a clitoris that superficially resembles a penis: elongated and pendulous yet stiffened by erectile tissue and an internal bone. The ring-tailed lemur’s clitoris is as thick and almost as long as the penis, with a urethra that sits within the shaft, allowing females to urinate from the tip, like a male. Ring-tailed females could ‘write their name in the snow’, joked Drea

A wide range of female mammals, from meerkats to the common garden mole, sport some degree of ‘masculinized’ genitalia. Most interesting to Drea 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.

This suggests to Drea that androgen-mediated female dominance could have been the ancestral state of not just lemurs but all primates, which includes us.

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. Lewis believes we need to find a new way of categorizing power structures to recognize the commanding influence of females that are small yet mighty.

As Lewis sees it, power can come from physical dominance or what she calls ‘economic leverage’. This could be specialist knowledge of where to find the best fruiting trees, controlling access to unfertilized eggs or strategic alliances. The celebrated Dutch primatologist Frans de Waal, professor of primate behaviour at Emory University in Atlanta, Georgia, agrees that female power is underrated. I caught up with him while he was in London and he told me about the far-reaching influence of Mama, the alpha female of a colony of captive chimpanzees he studied in Arnhem, Netherlands.

In chimps, the alpha male is officially the dominant political figure. But no alpha male could rise up and dominate the colony without Mama’s support, which gave her an enormous amount of power. The males may have sucked up attention with their screaming and fighting, but Mama was, without doubt, ‘the boss’.

Mama was broadly built and could be physically intimidating but de Waal noted she also had a sense of humour. She connected easily with all chimps, be they male or female, and developed a support network like no other in the colony. Mama was the top-ranking female of the troop, the alpha female – a position she held for over forty years, until her death. De Waal believes her status came from her unique charisma and social skills.