Women After All: Sex, Evolution, and the End of Male Supremacy (12 page)

Perhaps also: compliance. In many of these species, females dominate males in disputes over food and other resources, despite males being more aggressive. In our close cousins the bonobos, females control male aggression through alliances, not larger size, although there are other matriarchal species in which females are smaller than males. Perhaps the best explanation is that larger females breed better. This is certainly true of many insects and fish, and there is evidence for it in mammals.

But Ralls also reached a surprising conclusion: “Once female mammals became committed to internal gestation and lactation, their parental investment was so great that the likelihood of evolving a social system in which the relative parental investment of males exceeded that of females and males became a limiting resource for females became exceedingly slim.” In other words, once you go through pregnancy, you aren’t going to act like a female jacana. Although females in these mammals loom over and dominate males, they aren’t like jacanas, because even a doting mammal father is going to have a tough time catching up to the investment his mate has had to make before their young were born, as well as the ongoing investment she is committed
to biologically in producing milk. When the platypus genome was sequenced, this primitive egg-laying mammal turned out to have genes for three milk proteins matching our own, despite the fact that the platypus mom doesn’t even have nipples but secretes her milky fluid from modified sweat glands spread over her chest and belly. This means milk is as old as mammals—over 200 million years, to the common ancestor between us and the platypus—and later evolution did not cut back on mothering. Yet as we will see, some South American monkeys have fathers that invest so much they actually give mothers a run for their money.

Since Ralls’s pioneering work, we have learned a lot more about species in which females dominate males. She knew of some evidence that smaller males are favored in birds of prey because of greater hunting agility, and this has now been proved. Oliver Krüger’s sophisticated comparison of 237 species in the three main groups—falcons, hawks, and owls—failed to find a role for female competition or male agility in courtship, but it did strongly support the hunting hypothesis: in species that hunt more agile, rarer, and larger prey, males are smaller than females, because in these birds the little nimble males provide most of the females’ food while they incubate eggs and brood chicks. As Ralls thought, reproductive demands can keep females large.

Her work on mammals has also been brought up to date. A comprehensive 2011 review by Patrik Lindenfors and Birgitta Tullberg concluded that almost half of all mammals have males that are larger than females, “a pattern that is clearly linked to sexual selection.” Many fewer mammals have larger females, and there is little or no evidence that this reversal is due to sexual selection à la jacanas. So half of mammals have larger males, many have males and females who are the same size, and some have larger females, not because of competition for access to multiple fathers but because large size enables you to breed better in the ancient mammalian way. It also means you can defend resources, including your own
body, against male demands. But that doesn’t mean females don’t compete for males.

Ralls looked briefly at hyenas, and new research has shown them to be among the most fascinating of mammals, completely belying their negative reputation. Zoologist Kay Holekamp and her colleagues, looking back on their twenty-three years of research on Kenya’s spotted hyena in 2011, noted the great complexity and high level of cooperation in hyena society, including dominance hierarchies and coalitions resembling those of baboons. This favored unusual traits: “Adult females are larger and more aggressive than adult males, they are socially dominant to all adult males born elsewhere, and the female’s genitalia are heavily ‘masculinized.’ These unusual traits not only give females top priority of access to food, but they also give females virtually complete control over mating.” In the popular view, hyenas are nasty scavengers, while lions are glorious big-game hunters. In fact, hyenas, too, are top predators (killing 95 percent of their food, including the occasional human), and lions probably scavenge more than hyenas do. The two species often fight over a fresh carcass, whoever killed it. They have long shared habitats, as indicated by the thirty-thousand-year-old cave art of Lascaux and Chauvet.

However, females have very different roles in the two species.

Lionesses are smaller than lions and don’t sport gorgeous manes, but they do most of the hunting, often in small groups with their sisters. Males lounge around and eat—they are happy to take charge of a carcass killed by females—until strange males show up from out of the wild, in which case they will have to defend not only their life of leisure but also the cubs they have sired with the pride’s females. Foreign males will try to kill the cubs (over the usually vain protests of their mothers), and if the fathers can’t protect them either, those fathers will be driven out, often doomed, like the infants, by deadly wounds. In due course, the lionesses will mate and breed with the new males. Manes, by the way, cause overheating when
males hunt, but females nevertheless prefer the darkest and densest tresses. Males do feed their cubs on the meat they get, but it’s probably stolen from females or hyenas.

Hyenas, in contrast, live in a matriarchal world. Their large groups are collections of maternal kin, and female hierarchies are critically important. There is up to a fivefold difference in reproductive success between high-ranking females (who live longer, reproduce earlier, and have more surviving cubs) and their low-ranking counterparts, yet the least dominant female trumps the most dominant male. Males stay or leave on the basis of female choice, and when a male approaches a female in estrus to court her, biologically “ready” as she is, she may not be ready for
him,
so he is risking life and limb on his fond hopes. Both sexes are promiscuous, but the male is the supplicant and the female gets what she wants. Micaela Szykman and her colleagues closely observed many matings. In one, they reported,

Assumption of the receptive stance by the female appeared to signal the male that it was safe to mount her. After several pre-mounts, the male mounted the female, and repeatedly attempted to achieve intromission. This task was apparently made extremely difficult by the female’s peculiar genital morphology. The male had to squat down and under the female, so low that his rump was sometimes on the ground, to maneuver his erect penis into the female’s flaccid phallus.

Phallus? Or else call it a clitoris that prenatal hormones have hugely enlarged. The report explains further:

There is no external vagina, as the labia are fused to form a pseudoscrotum, and the clitoris is elongated and fully erectile such that it strongly resembles the male’s penis in size and structure. This pseudopenis is traversed to its tip by a central urogenital canal, through which the female urinates, copulates and gives birth. This unique
female morphology makes intromission by the male considerably more difficult than it is in other mammals and also makes copulation by force physically impossible. Although [she] retracts her clitoris into the abdomen to permit penetration by the male’s penis . . . the male hyena typically experiences unusual difficulty locating this opening and achieving intromission.

So the needy, fearful, disadvantaged males “must overcome unique motivational challenges associated with approaching and courting large, aggressive, well-armed females.” Female hyenas are
more
“masculine” than males in size, dominance, and fighting ability,
as
masculine in their genitalia, and yet bring life into the world and nurse their young. Males not only have to be fully approved to offer their dollop of genes, they often have to slide under the female, and rape is anatomically impossible.

These voyages around the world to look at how creatures great and small arrange their love lives are meant to help us think about our own historically fraught ways of doing things and, especially, to make us realize that male domination, however common, is not the only way and is no more natural than female dominance or, for that matter, equality. But there are very few systems where sex does not involve female choice. And today we can delve much more deeply into that pivotal process than was ever before possible.

The two most exciting trends in biology today are the close study of functioning brains and the rise of gene science. When you put them together to find out just how genes make brains make behavior, the thrill is doubled. Add to that the possibility of focusing these tools on closely related species that act quite differently, and you open new worlds of discovery.

Consider the small tropical fish studied by Molly Cummings of the University of Texas at Austin, described in her 2012 paper “Looking for Sexual Selection in the Female Brain.” She began
with a pair of closely related fish species that differ greatly in female choice: one has a lot of it, the other very little. Both have internal fertilization, which means the male must achieve physical intimacy with the female, and both bear live young, called fry.

The female-choice species is the El Abra pygmy swordtail, found in Mexico’s Río Pánuco. It’s a two-inch-long, sleek fish with dull greenish-brown scales, except for a black streak flanked by two rows of shiny blue stripes like arrow feathers. The male adds a long, thin black swordlike strand streaming along the bottom edge of an otherwise translucent tail fin. The male-coercion species, called the mosquito fish because it feasts on those insects’ larvae, lives in the Mississippi basin. It’s an iridescent yellowish-gray and about the size of the swordtail, except that the females are quite a bit larger than the males.

Cummings separated the sexes with a glass partition and let females stay as near a male as they liked. Swordtail males have a range of sizes; the smaller are less often chosen and (oddly enough) more coercive. Perhaps coercion stems from their size disadvantage, as it sometimes does in insecure human males. Females were exposed for half an hour to one of four choices: simple (between a large and a small male); minimal (two small males); same-sex (two size-matched females); and two empty compartments. Looking at the gene activity in their brains after this, Cummings zeroed in on four genes that turn on in the brain only during female choice, including in the females who chose between two small males.

Repeating all this with the mosquito fish, she did find some weaker preference for larger males, but the genes that were more active in female choice in swordtails were
less
active in female mosquito fish, which in the wild actually have
less
choice and
more
male coercion. Cummings reasoned that mosquito fish females might actually have to suppress their choosy brain genes to allow the rough mating process in their species to unfold—regrettable, but in their case reproductive.

The brain genes in question are found in many animals and have to do with remodeling brain circuits, one basis for learning and memory. Female choice in swordtails may be partly learned through experience with males, while mosquito fish may have to suppress the same learning process. Cummings is now trying to test this further by knocking down and overexpressing brain genes and then watching the females make their choices. The possibilities for transforming sex and courtship are mind-boggling.

Cummings was partly inspired by another comparison between closely related species that mate differently: the voles. The vole studies have been going on for over a quarter century—they were begun by Sue Carter and carried forward by Thomas Insel, Larry Young, and many others. First, Carter and her colleagues showed the importance of the now-famous brain chemical oxytocin in mothering. This provoked countless studies of oxytocin in attachment, friendship, and trust; even humans, when exposed to an oxytocin nasal spray that quickly reached the brain, became more sociable and trusting. Oxytocin has also been tried on people affected by autism, which is in large part a problem with social bonds. This ever-growing body of research was reviewed by Carter in 2014.

Oxytocin has created an exciting frontier in autism research, but it has also unveiled the basic biology of bonding. After working with Carter, Insel began comparing prairie voles, which are pair-bonding and paternal, with montane voles, which are multiple mating and only maternal. Male fidelity and fatherhood turned out to depend on a related brain chemical, vasopressin, but it was not the
level
of it that mattered—you could inject montane males with it and even then they wouldn’t commit. What counted was the location of receptors for it in the brain. That, in turn, depended on gene expression; the genes that made the receptors were switched on in key emotional circuits in the brains of prairie voles but not montane males. The switch is in the promoter for the gene, which can be long or short. In 2013 Zoe Donaldson and Young showed how the gene
controls the expression of the receptor in the limbic system, also known as the emotional brain.

Now comes the astonishing part. Because we know a lot about how to manipulate mouse genes, and because normal mice are neither pair-bonding nor paternal, Young’s lab put the prairie vole gene promoter (the long version) into male mice, and these remade males now wanted to hang out near females. Other vole species also fit the pattern: pine voles are pair-bonding and paternal, and the males match the prairie vole pattern of brain genes; meadow voles mimic the montane voles’ brains and behaviors. Yet Miranda Lim and her colleagues, doing the same kind of prairie vole gene insertion that Young had done with mice, made wayward meadow vole males into new men, in the prairie vole vein of loyalty and fatherhood. Their new genes made them family guys.

And not much of a gene change is needed—which helps explain why such similar species have such different mating habits. If some change in the environment gives pairing off and fathering a new advantage, evolution can almost flip a switch and produce (over many generations) a new mating system. And all this doesn’t just apply to voles. At present, Donaldson is exploring the same gene in primates to find out how all this works in some of our closest relatives. In chimpanzees, studied by William Hopkins, Donaldson, and Young, males with the short variant of the gene promoter were considered less dominant and more stable in their personalities than females. In 2014, Stephanie Anestis and her colleagues reported the first research on the gene in wild chimpanzees; they compared the wild population in the Kibale National Park, in Uganda, with those at the New Iberia Research Center, in Louisiana, and the chimps at the Yerkes primate center that Hopkins’s group had studied.