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Gentle sex? Females just as feisty as males over reproduction

Males compete for sex, females choose – ever since Darwin, we've assumed that's how nature works. Time for a rethink?
Gentle sex? Females just as feisty as males over reproduction

Damsels in control (Image: Richard Wilkinson

AFTER publishing On the Origin of Species, Darwin was worried. “The sight of a feather in a peacock’s tail, whenever I gaze at it, makes me sick!” he confessed in a letter to a colleague. His theory of natural selection, he realised, couldn’t explain why the males of some species have evolved such preposterous ornaments or why others have elaborate armoury. He needed another idea.

And so the theory of sexual selection was born. Males have weapons, Darwin proposed, to fight over females, and their bright colours, fancy songs and adornments were to seduce the reticent sex into mating. “The female, on the other hand, with the rarest exception, is less eager than the male,” he wrote. “She is coy, and may often be seen endeavouring for a long time to escape from the male.”

“89% Animal populations with polyandry”

Many of Darwin’s ideas caused great controversy among his Victorian contemporaries. But his ideas about sexual selection raised few eyebrows. The image of vigorous males competing for aloof, disinterested females fit the mindset of the time – at least that of men. Women’s opinions were rarely heard; few attended universities, let alone formal scientific meetings. , noted that woman is “the one animal in all creation about which man knows the least”. She also complained that science had been “exclusively made by men” and had “considered woman too often an absolutely passive being, without instincts or passions, or her own interests”.

Times have changed, but sexual selection theory has been slow to catch up. For a century, the idea gradually went out of fashion among biologists. Then, when interest began to revive, most of the new thinking was around males and whether they might use strategies other than fighting or flaunting to secure a female. There was talk of “mate guarding”, “sperm competition” and “ejaculate economics”. But the notion that males compete and females choose remained.

“1 in 5 Chicks fathered by cuckoldry”

“Undoubtedly, sexual selection has had a male bias,” says Geoff Parker at the University of Liverpool, UK, who helped bring Darwin’s theory out of obscurity. “Although I did warn early on that we should not see females as passive vehicles, I think I have been guilty of this too.” That bias is now being redressed, because evidence gained in recent years reveals that females, far from being coy, are just as keen on sex, and are equally competitive and aggressive – if the need arises.

As far back as the Ancient Greeks, people were aware that female animals might have sex with multiple partners. Aristotle noted that among chickens – seemingly the quintessential example of a dull harem dominated by a single sexy male – hens can mate with several cocks, a behaviour known as polyandry. So why did it take science so long to pay attention? For a start, the hen’s sexual antics are subtle. “Cocks openly fight and their crowing may be the first thing you hear every morning, while it’s much harder to figure out the pecking order among hens or catch them sneaking away to mate with other males,” says Tom Pizzari at the University of Oxford, who studies polyandry in the chicken’s wild ancestors. “But that doesn’t rule out a certain sociocultural bias in science.”

When the cock’s away

“When it comes to polyandry, I would agree that there’s been some wishful thinking, taking our own lofty norm to be the rule in nature,” says evolutionary ecologist Hanna Kokko at the University of Zurich in Switzerland. And hens aren’t the only birds we have misjudged. In the 1980s, technological advances shattered our illusions. “DNA fingerprinting made it possible to find out who’d fertilised the eggs,” says Kokko. “Many were shocked to discover that female birds weren’t faithful to their mates.” That birds should be revealed as promiscuous was particularly telling because about 90 per cent of species pair up, at least for the breeding season. Nevertheless, the DNA showed that as many as a fifth of the eggs produced by apparently monogamous females weren’t sired by their regular partner.

Following this unequivocal evidence of multiple mating, biologists have come to recognise that . In birds, they may be hedging their bets, trying to obtain better genes for their offspring while retaining the services of a faithful male to help look after their chicks. And in fish, where fertilisation normally happens outside a female’s body, and eggs may need to be guarded from predators, one male fish can take care of the eggs of many females. “That leaves females free to mate with several males, while males can be sure that they are investing time in their own broods,” says Suzanne Alonzo at the University of California, Santa Cruz.

Gentle sex? Females just as feisty as males over reproduction

Competition between female jumping spiders is very physical (Image: Mark Moffett/Minden Pictures)

Polyandry doesn’t just bring childcare and good genes, it can have more immediate rewards, too, such as nutritious gifts from males to enhance fertility. There’s even speculation that the same genes cause promiscuity in males and females alike. It’s no wonder it is common among invertebrates and widespread in vertebrates, including mammals. Given its prevalence, Kokko suggests, it would make more sense to consider having multiple sexual partners as standard for both sexes, and monogamy as the exception requiring explanation. “When you think of it, simply mating every time you meet an attractive male seems a much more straightforward strategy than mating once and then losing all interest,” she says.

But if females are just as eager to mate as males, why do they often lack ornaments and weaponry? . Because females tend to invest more heavily and for longer in producing offspring, the number of males that are ready to mate is usually higher, so competition for mates is more intense among males. That is especially the case when breeding females live in groups that individual males can monopolise. “Male deer, for example, have a lot to gain from winning fights – they may not get any matings if they don’t,” says Tim Clutton-Brock at the University of Cambridge. “Females, on the other hand, have a lot to lose – they’ll mate anyway, so why risk injuries?”

“90% Bird species that form “monogamous” bonds”

But successful reproduction is about more than scoring some sperm. Females also need resources to raise their offspring. And here things can get physical. “If the competition for food or nest sites is unusually intense, females can be the more aggressive sex,” says Clutton-Brock. “We see that in clownfish competing for anemones in which to live, in certain parrots vying for nest holes, and in meerkats.” He has spent decades studying meerkats in the Kalahari desert. Predation is common there and food is hard to come by, so adults group together to raise young, and females are stronger and fiercer than males. Some 90 per cent of infants descend from the dominant male and female. As a result, competition between females for the top spot is intense.

Sing when you’re winning

Among female birds, competition for resources can also be fierce. A nestful of chicks requires a lot of feeding, which is why a male and female commonly share the responsibility. But females can steal a march on the competition by getting a prime site to nest and forage in. To do this, they use a ploy that is normally associated with males: they sing. “, though they generally do so to defend a territory, not to attract mates,” says evolutionary ecologist Joseph Tobias at Imperial College London. “Especially in the tropics, where competition for territories is very intense, both sexes often sing together.”

“8 Average lifetime sexual partners, women”

All this leaves no doubt that reproductive competition can be just as intense between females as males. Out-dated sexual attitudes may partly explain why it has taken some biologists so long to come to terms with this. But there are practical reasons, too. “Not only is the frequency and intensity of female aggression usually lower,” says Clutton-Brock, “but females are also much harder to recognise individually, because there are often many more females than males around, they tend to look more similar, and they often do not exhibit any obvious scars.” Also, field studies are needed to compare the long-term reproductive success of females.

“12 Average lifetime sexual partners, men”

Now that we are starting to overcome these issues, some believe we need to overhaul Darwin’s theory of sexual selection. “Sexual selection is broken, it’s worthless and it’s harmful,” says ecologist Joan Roughgarden of Stanford University in California. She favours the idea of social selection, based on group behaviour rather than that of individuals. But most think the theory needs evolution not revolution. Clutton-Brock, who was among the first to call for sexual selection to include female-female competition, says: “What’s happened in the last 20 years or so is that scientists, including us, have been focusing on exceptions. Those are very interesting, but we should not forget they are exceptions.” What these exceptions do give us, however, is a more balanced view of the mating game – one that may even shed light on our own behaviour.

. “While males are forming coalitions, females are often by themselves, and compete for exclusive access to fragments of forest where lots of food can be found,” says Anne Pusey, who studies chimps in Gombe National Park, Tanzania. Overt aggression is rare, but infants are at risk of being killed by females who aren’t their mothers. There is one situation in which competition is inevitable. “Male chimps don’t migrate – they’d simply be killed when found in the forest all by themselves,” says Pusey. “Females usually do, and immigrants are under relentless attack by the other females until a male steps in to protect the cute new girl on the block.”

That is similar to what may happen when competition for partners and resources becomes intense in humans, says psychologist Anne Campbell at the University of Durham, UK, . “Good male partners can be very thin on the ground [in these areas] – male mortality is high, many men end up in jail, and the ones who are successful will often leave the neighbourhood,” she says. Here the most desirable men are often gang members who have money and status. “They can provide for their girl, but since they’re spoilt for choice, they can also afford to treat the girls quite abusively,” says Campbell. “Yet, because of the intense competition for male partners, girls tend not to band together to teach those guys a lesson, but take it out on each other – especially on the new girls.”

Campbell’s work has upset some evolutionary psychologists and those who believe that the world would be at peace if women were in charge. She takes a more detached view. “Even though biology may help us understand where some of our more unpleasant tendencies come from, it never prescribes how things ought to be,” she says. “On the contrary, I think understanding why people may feel or act this way may help us to deal with it.”

And the same goes for men, of course. “If anything, biology discourages me from being too much of a dominant male,” says Clutton-Brock. “You see male behaviour all the time that is unnecessary and unpleasant, in animals and elsewhere. We should be able to do better than that.”

Sisters are doing it for themselves

Gentle sex? Females just as feisty as males over reproduction
Matriarchs rule the roost and inherit the family wealth among the Mosuo in China (Image: Patrick Aventurier/Gamma)

Throughout history and across the globe, many cultures and most world religions have tried to impose lifelong monogamy – on women, at least. “Female monogamy is enforced in most so-called patrilineal societies, where wealth can be easily accumulated and only men inherit from their parents,” says Ruth Mace at University College London. “In that case, it’s quite important to make sure your heirs are your sons and not someone else’s.” Among the hundreds of societies that exist today, just a few dozen are matrilineal, with daughters inheriting.

Competitive parenting

In recent years, Mace has been studying one such group, the Mosuo of south-western China. They live in communal households, with a matriarch and several generations of her family under the same roof.

. But no matter how long-term the relationship, the men remain in their own family homes, where they help care for the children of their sisters and nieces and may never pay much attention to their own offspring.

In this matrilineal society, family wealth, which comes mainly from farming, stays within the household. Nevertheless, sisters must share these limited resources if they are to reproduce, and .

Mace’s analyses of historical and current data describing all the births and deaths in Mosuo families show that the more older sisters a women has, the fewer children she will produce. How this “reproductive competition” actually unfolds is unclear. “Infant mortality is low, harmony is considered very important, and family relations appear quite peaceful, so it’s probably something rather subtle,” says Mace. “Like most people, the Mosuo don’t like to answer indiscreet questions about their sex lives.”

Topics: Biology / Evolution