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Lucy Cooke was in the Serengeti, making a BBC documentary about animal communication, when the lion expert in the Jeep with her played the sound of a roar from another lion’s territory. Three lions, two males and one female, approached. The two males disappeared when they saw there was nothing that resembled a rival. But the female lion pinned them, circling the Jeep. They were stuck for two hours. What was going on? Cooke was informed the female wanted to mate with them. “That female lion—she’s incredibly promiscuous,” the lion expert told her. “She’ll mate up to a hundred times with multiple males during her fertile period.”
This blew Cooke’s mind. “I was thrilled and quite delighted by the licentious promiscuity of the lioness,” Cooke told Nautilus in a recent conversation. That’s when the seed of her new book, Bitch: On the Female of the Species (or, in the United Kingdom edition, A Revolutionary Guide to Sex, Evolution, and the Female Animal) was planted. Cooke calls it a “shocking revelation” to have learned that “much of what I had been taught as gospel at university, the very foundations of evolutionary biology, had been distorted by prejudice.” At Oxford University, where Cooke earned her master’s in zoology, she was taught that, almost as a matter of biological law, males were the promiscuous ones, and females were choosy and chaste. The idea dates back to Charles Darwin’s theory of sexual selection, and Bitch is about bringing Darwin up to date. (“This isn’t your grandfather’s evolutionary biology,” the book’s online description reads.)
“His theory of sexual selection was infused with the chauvinism of the period, unfortunately, which was very surprising to me, because Darwin’s my hero,” Cooke said. “He’s the reason why I studied evolution. He is an extraordinary, meticulous scientist. It’s fascinating that someone who is as cautious and thorough and methodical as Darwin is also not immune to cultural bias.”
Bitch is an entertaining and erudite corrective to years of research bias against the idea of female agency in evolution and the study of female sexual anatomy. During our conversation, Cooke was jovial, and talked a lot about sex—duck sex, dolphin sex, spider sex, as well as same-sex “GG rubbing” among bonobos. She explained why sex didn’t evolve for just reproduction (“another real Victorian idea”). She also talked about what it might mean for humanity that bonobos were able to “overthrow the patriarchy through ecstatic sex.”
What was your impetus to write Bitch?
We are living in a time where being female has never been more scrutinized or politicized. I feel that there’s been a revolution in our understanding of what it means to be female. And that revolution started in the early 1980s with the likes of Sarah Hrdy and Patricia Gowaty first challenging these stereotypes that Darwin had set in stone of the passive female that’s chaste, submissive, and coy. But even though they started those challenges and, in many cases, won them in as early as the 1980s, much of that thinking has taken a long time to permeate into popular culture and even into science.
Is there one insight in particular that you want to leave readers with?
What I would hope is people understand that biological sex isn’t a crystal ball. Females are not meant to behave in a certain way because they produce eggs. Males are not meant to behave in a certain way because they produce sperm. The variety that we see in nature of both the expression of sex and the spectrum of sex itself, should inspire us to see the limitless possibilities of the female experience, and not feel boxed in by stereotypes.
Gowaty, who’s been questioning these stereotypes for 30-odd years now, has taken to task Angus Bateman’s study, a fruit fly experiment in the 1940s. It underpinned the stereotypes that females had nothing to gain by mating with multiple males. Whereas males have everything to gain. This was part of a law that held that males are promiscuous and females are chaste.
Gowaty has taken a forensic scalpel to Bateman’s study, reproduced it herself, and gone back to his original notes, and found that even his own data doesn’t support his results. He suffered from a case of confirmation bias. He skewed the results, and he collated them in a way which substantiated what he wanted to see rather than what was in front of his eyes.
The foundations of evolutionary biology had been distorted by prejudice.
Why do you describe sex, as in the male and female categories in species, as anarchical?
I was really surprised when I came to understand how sexual differentiation actually happens. Everybody at school learns that males are XY and females are XX. You think that the genes that govern being male are on the Y chromosome, and the genes that cover being female are on the X, and that the pathways that take you to being male or female are linear and distinct. That’s what I assumed, like many people. And then I spoke to Jenny Graves, who had been studying sexual differentiation and determination for a very long time, in everything from platypus to nematode worms. She was part of the team that found the SRY gene, which is of course the trigger for the male pathway in humans. She’s the one who told me that it’s a pretty anarchic setup.
I was amazed by what she told me. When you have a fetus, it starts off as sexually neutral with a unisex kit of parts. Then there’s a trigger—in humans, the presence or absence of the SRY gene—that starts one of these two pathways. The gonads either start down the pathway of becoming a testes or an ovary. Now, what I didn’t know, which Jenny told me—she had to tell me three times because I couldn’t believe it—is that the genes involved in making testes or ovaries are basically the same 60 genes. They just play to a different tune. And these two pathways involving these 60 genes are neither separate nor linear. They’re enmeshed, and they work antagonistically. So, to create an ovary, you have to suppress the testes at the same time.
They’ve now found in studies of mice that this suppression, this antagonistic relationship between these two pathways, continues into adulthood, which suggests that the gonad is never actually stable in a mouse, an astonishing thing to discover. When she sent me this diagram to explain what these two linear pathways look like, it was like a machine of millions of cogs with these little blue balls being spat out and pumped between things, and destroyed, and the whole thing was like a whirring map. It was chaos. She said that’s what she sees these pathways to be like. This anarchic system is why you get such extraordinary variation.
What’s an example of an animal that epitomizes this extraordinary variation?
The common garden mole. A couple of years ago, it had its genome decoded. The common garden mole female has what’s described as “ovotestes.” Her gonads are part ovarian tissue and part testicular tissue. During the breeding season, her ovarian side produces eggs. She has a pregnancy and gives birth as you’d expect. But outside of the breeding season, the testicular tissue swells, and it produces testosterone. Doesn’t produce sperm, but the testosterone makes her dig really hard, and be really aggressive. It also means that she has a vagina that’s sealed shut, and her genitalia externally resemble a male. She has a clitoris that looks like a penis. So, she’s pumped full of testosterone. Morphologically, she looks, externally, like a male, yet she is a female. That sort of gonadal flexibility is the result of an incredibly anarchic system involving androgynous genes.
Evolution has furnished the male barnacle with an extravagantly long penis.
So what fundamentally tells men and women apart?
Biological sex is the standard definition. That’s what the gonads do. Egg-making as opposed to sperm-making. But even that definition is problematic when you see creatures like the mole, and like common garden frogs. They have genetic sex determination. But then that genetic sex determination can be overridden by an environmental sex determination. There are plenty of animals, reptiles, and amphibians, that have environmental sex determination. Famously turtles: If they’re incubated over a certain temperature, they become female. Under that temperature, they become male. Frogs, it looks like they also have some sort of environmental trigger. Not sure what it is. But it can override the genetic trigger. You end up with XX males and XY females. Their gonads are a mishmash.
It was amusing how you described the way Darwin talked about the barnacles finding mates. Because barnacles don’t, or can’t, move.
Well, you’re right. If you’re a barnacle, you are cemented to a rock with your head. One of Darwin’s big contributions to the field was realizing that barnacles were crustaceans, not mollusks. They’re like crabs and lobsters, but they’ve eschewed their mobility for home security. That’s what barnacles are big on. Their juveniles will form calcified plates and attach themselves to a rock by their head. Bingo for home security! Less good for finding a mate.
But thankfully, evolution has furnished the male barnacle with an extravagantly long penis. It’s several times longer than his body. He can cruise the neighborhood for sex without ever having to move and inseminate whoever he comes across, and also make the best of a situation where if he can’t find anyone to fertilize, he can just come home and fertilize himself.
Dolphin sex is very much unlike barnacle sex. The mating involves lots of movement. How has female sexual anatomy adapted?
This is new research from Patricia Brennan, who operates out of Mount Holyoke College in Massachusetts. Patricia is really the first person to study vaginas. Penises have been studied for a very long time because there’s extraordinary diversity out there. Animal penises can have spines, bones, corkscrews. They can be roving, lengthy objects, like the barnacles. Taxonomists even use genitalia as a means of telling apart species that are otherwise identical. Certain beetle species can only be told apart by looking at their genitals. And so there’s been a huge fascination in penises in zoology for a long time. Less so for vaginas.
Now, you could say, “Oh, it’s inside. It’s harder to examine.” But the reality is that female genitalia was thought of like females were thought of—as being just a passive receptacle for the male. But Patricia Brennan has thought otherwise and has studied them. She paid attention to the genitalia of ducks first. Male ducks are famous for having, like the barnacle, a ridiculously long penis. I think the Argentine lake duck has one even longer than its body. On top of that, it’s a corkscrew. You might think to yourself, “Well, I’ve never seen that on a duck.”
I was actually thinking that.
Most of the time, it’s kind of kept inside the cloaca. Ducks, and all birds, have cloacas. In the case of ducks, they also have this penis inside the cloaca that is filled with lymphatic fluid and can explode out of the cloaca at something like 75 miles an hour, like a sort of sinewy party hoot. You know those party hooter things you get, that shoot out? This extraordinary organ has caused a bit of a stir. And there’s been lots of theories as to why duck penises would be so long and corkscrew. The idea was that it was good old sexual selection. Male competition. Unfortunately, young males that don’t find a partner gang up together, and they can be sexually coercive on females. It’s a really horrible thing if you’ve seen it. That was the driving force of the male penis length. The idea was that the longer the penis, the better able the male that wins the fight is at getting his sperm in.
Patricia Brennan was the first person to say, “Well, I wonder what kind of garage he’s parking his car in?” She looked inside the female duck, which the textbooks would tell you is just a simple tube. She found anything but a simple tube. She found just as extravagant an organ. It corkscrewed in the opposite direction.
It makes evolutionary sense for males to get eaten.
Why would the duck vagina evolve that sort of structure?
What Patricia realized is that it prevents coercive males from fertilizing her, because a female vagina of a duck can open wide in order to lay an egg. The lumen can expand to lay an egg. Patricia theorizes that the female, if she chooses her partner in an elaborate dance, and he’s the one that she wants to fertilize her egg, then she’ll open up the lumen of her vagina, and this weird, curly whirly penis will go all the way through.
And if she’s not interested?
Then her vagina remains tight. And with all these blind pouches, and this corkscrew the opposite way, the male’s penis often folds back on itself and doesn’t fertilize the eggs. That supports the data, which was always anomalous before: Very few of these coercive acts ever result in chicks.
Why is it evolutionarily significant that very few acts of forced duck sex result in chicks?
What was fascinating about that is that it’s the female that’s driving the evolution of the extraordinary male penis. Patricia Brennan also rescues the female from being a victim in all of this because she’s retaining her autonomy. She’s choosing who fathers her egg, although she’s still subject to coercive acts. But as far as evolution’s concerned, she’s the winner, because she’s retaining the choice of who fertilizes those eggs. Dolphins are also famously coercive, but Patricia found the same convoluted vagina, and she thinks it’s the same deal there.
How did sex evolve to be more than just a way to reproduce?
This is another real Victorian idea, that sex is just for reproduction. If sex is just for reproduction, then same-sex sexual activity becomes anomalous. Because it’s like, “Well, that’s a waste of energy, isn’t it? Why would that happen?” Yet same-sex sexual activity is widespread in the animal kingdom. Bruce Bagemihl, author of Biological Exuberance: Animal Homosexuality and Natural Diversity, documented over 300 species where same-sex sexual activity has been observed. In particular the bonobos, who are our closest relative alongside chimpanzees—the females have sex with each other. It’s called GG rubbing. Their clitoris is migrated, so that it’s in a position where it gets the most stimulation from this particular kind of sex. Amy Parish, who studied female bonobos, told me that if a female and a male present themselves to a female bonobo, more often than not, she’ll choose to have sex with a female. The reason why this sex is so prevalent is because it serves a function, which is that it bonds the females.
You’d expect them to be competitive with one another. Female bonobos are like chimpanzees. They don’t form a stable heritable matriline in groups. They are the sex that disperses from their natal group. So, when females are together in troops, they are unrelated females. Yet they’re not competitive with each other. They have this incredibly strong sisterhood, which is forged and maintained by sexual activity with each other, which basically dampens aggression.
As a result of those bonds, the females are the dominant sex. Male bonobos are like chimpanzees. They’re bigger than females. But they’re not the dominant sex. The female bonobos eat first, whereas female chimpanzees don’t. In most situations in the wild and all situations in captivity, females are dominant. So, the female bonobo have basically overthrown the patriarchy through ecstatic sex.
How come bonobos were able to overthrow the patriarchy through sex, and the chimpanzees weren’t?
It’ll be the environment. That’s what it is. Chimpanzees are much more widely distributed in Africa than bonobos. Bonobos are only found on one side of the Congo River in a fairly small area. I believe there’s more abundant fruit where they live. Chance is another factor. But it is interesting that they are so radically different, because male chimpanzees are patriarchal and warlike. Bonobos, equally closely related to us, are matriarchal and peaceful. Until the bonobo came along, the chimpanzee was the model for our ancestry as our closest relative. Then the bonobo came along and suddenly, “Oh, could that be a model for our ancestry?” That’s the kind of thing that anthropologists will argue about forever.
Does the story of the chimps and bonobos illustrate the flexibility of dominance?
Yes. It’s not dictated by whether you produce eggs or sperm. Patriarchy isn’t burnt into our primate DNA. It’s flexible. It also shows the power of the sisterhood. I’m not suggesting that we all have sex with each other. But forming alliances with females is clearly a good thing if you want to gain power. And it also shows the flexibility of sexuality. All bonobos, essentially, are bisexual. They’re quite happy. It doesn’t really matter. You can draw what you like from that.
“Well, I wonder what kind of garage he’s parking his car in?”
What are the forces that determine how sexual dimorphism works in different species?
Darwin would’ve said that those dimorphisms are dictated by our sex cells. Females produce small amounts of energy-expensive eggs. And so we are destined to be choosy and chaste, and passive. Whereas males produce lots of mobile sperm, and so they’re destined to be active and big, aggressive and dominant. But what we now understand is that sex isn’t a crystal ball. Whether you produce eggs or sperm, it doesn’t dictate what kind of dimorphisms exist, if any. It’s the environment that you find yourself in that does. It’s the combination of environmental factors, shared genes, and a bit of serendipity. There’s also a considerable element of chance that shapes sexes to be either the same or different. But it’s not simply that you can equate males are going to be bigger and more aggressive because they produce sperm, and females are going to be small and passive because they produce eggs. It’s just nonsense.
Do you think Darwin was trying to avoid controversy in his treatment of sexual selection? Because his theory of natural selection was so radical. It challenged religion, and ideas of creation. Sexual selection, on the other hand, seems much more conservative, seemingly enshrining the Victorian values of English culture. Is that how you see it?
Well, this is a fantastic discussion to have and one that I really enjoy because it is all conjecture really, at this stage. But there are clues, aren’t there, in his other writing? His two big published books, On the Origin of Species and The Descent of Man—they are a lot more conservative than, say, his more obscure monographs on barnacles. And so it’s difficult to work out, isn’t it, is how liberal he was? “What was his thinking? Did he really believe that females were inferior to males, and that males were the dominant drivers of evolutionary change?”
Well, I think he did believe in his theory of sexual selection, that it was driven by male competition and female choice. And he gave females agency by suggesting that female choice could shape the evolution of males. And that went down like a lead balloon in Victorian England. In that way, he did give females agency. His daughter, Henrietta, edited the book. She was famously prudish. So, how much she constrained his writing, we don’t know. But I agree with you. To anger the church and suggest that humans had evolved from primates—that’s probably enough controversy in one lifetime. He might not have been striving for sexual equality in the wake of that.
Listening to you narrating your book on my phone, I could tell you must have really enjoyed researching and writing about spiders.
It’s just so amazing, isn’t it, to imagine that world? Females can be way bigger, like 125 times bigger than the male, which is astonishing. The females also live much longer. The males live for a fraction of a time. Sometimes, they don’t have fangs or even venom. They’re just walking sacks of sperm. Also, to cap it all, they look like lunch. It makes sense for the female to be bigger. Because she’s bigger, she can make more eggs. Although they’ve got eight eyes, they don’t see very well. Their main sense is vibration. That’s how they detect almost everything. So, if you are a male spider, you want to get the attention of your mate. She can’t hear. She can’t necessarily see you. So, you’ve got to make vibrations. And the best way to get her attention is to make like dinner, and shake the web, and be like, “Woo.” Like, “Whoa, dinner.”
Because animals with small brains have a limited sensory realm, so many courtship routines are based around things that are a bit like food. With bowerbirds, for example, the ones that decorate their bow with blue bling, well, that’s because there’s a blue fruit that’s much prized. The male has to make like dinner to get noticed, because the worst thing that can happen is that he doesn’t mate at all. He might get eaten before. If she’s hungry and he’s played it badly, he might get eaten before sex. But even if he gets eaten during sex, which often happens, they can be incredibly fast with their pedipalps, which inserts the sperm. Everyone’s a winner. Not only has the male managed to fertilize the female, but by eating his body, she’s also going to nourish those eggs and spiderlings. And they’ve got a better chance of survival.
That seems brutal.
But it works. It makes evolutionary sense for males to get eaten. Eileen Hebets, who studies in Nebraska, does some amazing work on spiders. She’s found that there is something particular about eating another member of your own species that’s particularly nourishing for the female. The females that cannibalized their own species grew much bigger and did much better. So, she came to the conclusion that there’s something uniquely nutritious about eating your own species. But life’s not great for the female spider because matriphagy is a thing with spiders. The mother herself may end up being consumed by her spiderlings, slowly eaten, abdomen first. 
Brian Gallagher is an associate editor at Nautilus. Follow him on Twitter @bsgallagher.
Lead image: Gudkov Andrey / Shutterstock
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