It was a moment that smashed assumptions with the force of a wrecking ball. She approached the sexy older male who seemed to arrive from out of nowhere, his black-and-white coat gleaming in the light. She put herself directly in his path, shook her head provocatively, then turned and bent over to “present” herself to him. She eagerly pressed her backside against his groin and the two gyrated against each other. Spectators watched as the two built toward a climax, and then they went their separate ways. The sexual display took the scientific community completely by surprise.
When primatologist Sarah Hrdy described this behavior among female hanuman langurs—or Semnopithecus entellus, a monkey species from western India—in the late 1970s, it erupted into the kind of controversy usually reserved for lewd performances at the MTV Video Music Awards. Ever since Darwin there had been an assumption among evolutionary biologists that females were coy and choosy in their sexual behavior while males were the ardent, promiscuous sex. Even though important advances in gender equality have been achieved since then, “most Darwinian models of human origins incorporate females only as passive objects of male competition,” wrote biological anthropologists Craig Stanford and John Allen as the 20th century came to a close. And yet these female langurs were observed actively pursuing males from neighboring troops while, according to the prevailing theory, they should have been chaste rather than chasing. What was even more surprising was that they would exhibit these sexual advances at any stage in their estrous cycle, sometimes even when they were already pregnant.
“Under some circumstances,” Hrdy wrote in her classic 1977 book The Langurs of Abu, “females are continuously sexually receptive, a pattern previously thought to occur only among human females.” Primatologists refer to langur societies as polygynous, in that they are composed of multifemale, single-male groups. Darwin’s theory of sexual selection held that these females should choose the most impressive male in their troop to ensure the hereditary success of their offspring. But here was clear evidence that females would actively engage in “adulterous solicitations” with males from other societies. As Hrdy revealed to a scandalized scientific community, the genetic benefits that came from seeking extra-pair matings—while maintaining the support of an existing partner—meant that evolution could favor females who choose to cheat.
More than 30 years of subsequent research has confirmed Hrdy’s findings and expanded on them to reveal that females in many primate species, humans included, engage in a diversity of sexual strategies to enhance their overall reproductive success. For example, in saddle-backed tamarins, females will solicit sex from multiple males who will each help to care for her offspring.* Female mouse lemurs will mate with up to seven males during a single night. Capuchin monkeys will seek out mating opportunities in the early stages of their pregnancy, presumably to confuse males about paternity. And bonobo females will have sex with everybody at pretty much any time they feel like it.
In the latest addition, Brooke Scelza, a human behavioral ecologist at the University of California–Los Angeles, contends in Evolutionary Anthropology that not only do human females seek out multiple sexual partners as an evolutionary strategy, they opportunistically shift that strategy depending on the environmental context (more on that below). In other words, female sexuality is not so much blindly promiscuous as it is pragmatic.
Of course, in an earlier era the scientific paradigm for understanding sex was much more rigid. In 1948, a balding and near-sighted English geneticist by the name of Angus Bateman published one of the most influential papers ever written on the evolution of sexual behavior. After studying patterns of inheritance among offspring in the common fruit fly, Drosophila melanogaster, Bateman concluded that the division between ardent males and coy females was “an almost universal attribute of sexual reproduction” across the entire animal kingdom. Bateman reasoned that, because females produce dramatically fewer eggs than males do sperm, and because eggs were physiologically more expensive, female reproductive success would not increase by mating with more than one male. Instead, females should focus on choosing the “best” male that they could and then directing their energy toward raising offspring. On the other hand, males who mated with multiple females would be expected to greatly increase their own reproductive success because the benefit outweighed the cost of production. Sex, like economics, was a question of quantity versus quality.
There was only one problem: Bateman got it wrong. In June 2012, UCLA biologist Patricia Gowaty and colleagues replicated Bateman’s study only to find that he had come to faulty conclusions because his methodology was severely flawed. Without modern genetic analysis at his disposal, Bateman conducted his trials with males and females of known mutant strains whose offspring could be easily identified. However, he counted only offspring that had two mutations—one from each parent—in order to be certain of a given fly’s reproductive success. This approach resulted in a biased sample because flies with some mutations were less likely to survive than those with others. In the end, the premiere study on sexual selection—which had been cited by more than 2,000 peer-reviewed papers and textbooks—contained a fatal flaw that would have been easily identified had the study been replicated sometime in the preceding 64 years. How could this happen?
“Our worldviews constrain our imaginations,” Gowaty said after her study was published in the Proceedings for the National Academy of Sciences. “For some people, Bateman's result was so comforting that it wasn't worth challenging. I think people just accepted it.” The uncomfortable implication is that Bateman’s paradigm was so widely cited because it conformed to assumptions about how female sexuality ought to be. These assumptions were constructed over a long history and had infiltrated Western culture so completely as to be nearly invisible.
* * *
For many European explorers, the New World was a blank slate upon which they could write anew, if only it weren’t for the millions of people who already lived there. In 1633, the French missionary Paul Le Jeune wrote from northeastern Canada to his Jesuit order about the great difficulties he had in converting the indigenous Montagnais people to Christianity. “The inconstancy of marriages and the facility with which they divorce each other, are a great obstacle to the Faith of Jesus Christ,” he complained. However, what was even more alarming to Le Jeune’s Christian sensibilities was the tendency of married women and men to take lovers, many of whom would openly raise together the children from these affairs. In one telling exchange with the village shaman, Le Jeune condemned such “savage” and “licentious” behavior:
I told him that it was not honorable for a woman to love any one else except her husband; and that, this evil being among them, he himself was not sure that his son, who was there present, was his son. He replied, “Thou hast no sense. You French people love only your own children; but we all love all the children of our tribe.” I began to laugh, seeing that he philosophized in horse and mule fashion.
The anthropological literature has a rich tradition of privileged white men expressing shock and indignation over the sexual behavior of other cultures. However, even from the field’s inception, it was well understood that Western-style monogamy was anything but the norm. The American ethnographer Lewis Henry Morgan, for example, wrote in his 1877 book Ancient Society that a flexible marriage system was common for “primitive” societies and was one that “recognized promiscuity within defined limits.” Morgan’s work was so highly influential at the time that Darwin was forced to admit in The Descent of Man, “It seems certain that the habit of marriage has been gradually developed, and that almost promiscuous intercourse was once extremely common throughout the world.”
Despite this early acknowledgement that human societies had a range of approaches to sexual fidelity, few researchers chose to pursue the question from a woman’s perspective. As a result, as late as 1982, Donald Symons, an anthropologist and early founder of evolutionary psychology, could write that there was “dubious evidence that this [assertive sexual female] nature exists and no evidence that women anywhere normally tie up multiple male parental investments.”
The village networks in the Omuhonga basin of northwestern Namibia would prove such ideas about female agency wrong. It was here, surrounded by giant acacia trees, that anthropologist Brooke Scelza interviewed married women among the Himba, seminomadic pastoral people who live almost exclusively on livestock. These Himba women, their skin and elaborate braids beautifully decorated in red pigment made from crushed ochre and animal fat, would be entered into arranged marriages at a young age. However, as Scelza discovered, while their husbands traveled long distances managing the herds, female adultery was commonplace back home. Out of 110 women interviewed, fully one-third said that they sought out extramarital affairs that resulted in the birth of at least one child. Because there is no social stigma attached to these liaisons in Himba society, both women and men discuss them openly. (Divorce can likewise be initiated by either party.) As a result, according to Scelza’s analysis published in the journal Biology Letters in 2011, “women who had at least one extra-pair birth have significantly higher reproductive success than women with none.”
Of course, this was certainly not the first time that extra-pair paternity had been connected to female reproductive success. Previous studies have reported evidence of female infidelity in small-scale societies such as the !Kung of South Africa, the Ekiti of Nigeria, the Vanatinai of New Guinea, the Tiwi of Northern Australia, the Tsimane of Bolivia, and the Yanomami of Brazil. In addition, 53 societies can be classified as having systems of “informal polyandry” in which women have simultaneous sexual relationships with more than one man. In many South American societies, such as the Ache, Bari, Canela, Mundurucu, and Mehinaku, it is believed that it takes the semen of several men to produce a baby. In two of these “partible paternity” societies, the Ache and Bari, children with more than one father were found to have lower mortality and improved nutrition due to a greater level of provisioning. When anthropologists Kim Hill and A. Magdalena Hurtado asked 321 Ache about their kinship information, the total included 632 fathers, or an average of two “fathers” each. This is perhaps not so different from the common situation of American children who receive support from both their biological father and current stepfather. As long as the biological father contributes support, such children might well gain by having two fathers.
While a great diversity of sexual norms exist around the world, ranging from strictly enforced monogamy to polyamory, according to Scelza’s new study there are two environmental contexts where women commonly choose multiple partners. The first is where women have more material support from their kin or economic independence from men more generally. This may explain why multiple mating is most common among small-scale matrilocal societies (in which women remain in their home village after marriage), such as the partible paternity societies of South America or the Mosuo of China. It may also explain why female infidelity has increased in Western societies as women have gained greater political and economic independence. (For example, Iceland was ranked first in gender equality by the World Economic Forum in 2013 at the same time that 67 percent of children were born out of wedlock, the highest rate in the Western world.) Under this scenario, women choose multiple partners because they have more options available to them, they can rely on their support network during transitional times, and they have greater personal autonomy.
The second environmental context Scelza identified is where the sex ratio is female-biased (indicating a scarcity of men) or there is a high level of male unemployment (indicating a scarcity of men who can provide support). Women may be trying to “make the best of a bad situation and capitalizing on their youth to improve their reproductive prospects.” In such environments women tend to have higher rates of teen pregnancy as well as illegitimate births. Multiple mating may be a way of hedging their bets in an unstable environment. By pursuing an ardent sexual strategy, women are able to choose the best potential males as well as gain the support they need in order to maximize their reproductive success.
In many societies today, including our own, women who are overtly sexual and pursue multiple male partners often experience moral outrage and “slut shaming” of a kind that is entirely unheard of in other parts of the world. While these cultural attitudes used to look toward science for justification, that position is becoming increasingly difficult to reconcile with the biological evidence. From Sarah Hrdy’s discoveries among the langurs of Abu to polyamorous meetups in Aberdeen, female sexuality has been revealed to be a far more dynamic area of research than Darwin could have imagined. As Hrdy stated herself in the Annals of the New York Academy of Sciences at the dawn of the 21st century, far from being passive, females are “flexible and opportunistic individuals who confront recurring reproductive dilemmas and tradeoffs within a world of shifting options.” Or, as another observer summarized, “It’s our party. We can love who we want.”
This is the first in an ongoing series of columns that Eric Michael Johnson will be writing for Slate on the ways that evolution impacts our lives today.
Correction, Dec. 5, 2013: This article originally stated that saddle-backed tamarins are socially monogamous. Recent research has shown that they are not.