The Primate Diaries

The Primate Diaries

Notes on science, politics, and history from a primate in the human zoo.

Helen’s Choice: Female Multiple Mating in the Natural World


"Helen of Troy" by Nathaniel Gold

“Helen would never have yielded herself to a man from a foreign country, if she had known that the sons of Achaeans would come after her and bring her back. Heaven put it in her heart to do wrong, and she gave no thought to that sin, which has been the source of all our sorrows.”

- Homer, The Odyssey

“[A] male's reproductive success depends on how many females he mates with, but not vice versa; for a female, one mating per pregnancy is enough. That makes females more discriminating in their choice of sexual partners.”

- Steven Pinker, "Why Can’t A Woman Be More Like A Man"

Classical literature condemned Helen of Troy for a crime against nature. Because she chose Paris, after having children with Menelaus, one of the great cities of the ancient world was destroyed. Modern behavioral ecology, while somewhat less melodramatic, has likewise had difficulty accepting a promiscuous female strategy as a factor in evolution. Whereas male strategy has long been considered inherently virile and ardent, females are described as coy, discriminating, reluctant, and demure. In an article I wrote for Slate last week I highlighted the premiere study that upheld this dichotomy, a 1948 paper by British geneticist Angus Bateman cited in more than 2,000 journals and textbooks.

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.

Charles Darwin initiated the theory of sexual selection that Bateman based his assumptions on and it is a framework that has remained largely unchanged to this day. As Darwin wrote in On the Origin of Species (1859), “Amongst many animals, sexual selection will give its aid to ordinary selection, by assuring to the most vigorous and best adapted males the greatest number of offspring. Sexual selection will also give characters useful to the males alone, in their struggles with other males.” While Darwin wrote little about sexual selection in his first book the examples he did provide argued well for his initial premise, including male alligators “fighting, bellowing, and whirling round, like Indians in a war-dance, for the possession of the females,” male salmons “fighting all day long” in mate competition and male stag-beetles that “often bear wounds from the huge mandibles of other males” as they battle over sexual access.

This line of reasoning was followed, just over a hundred years later, with E.O. Wilson’s argument in Sociobiology (1975) that, “the courted sex, usually the female, will therefore find it strongly advantageous to distinguish the really fit from the pretended fit. Consequently, there will be a strong tendency for the courted sex to develop coyness.” From this it follows that females are passive players in the evolutionary struggle who, much like The Odyssey’s Penelope, must demurely choose between the most superior of her male suitors.

However, instead of the Bateman paradigm, consider the case of another fruit fly: Drosophila bifurca. In this species the males produce sperm that are twenty times longer than their total body size. For humans this would be the equivalent of a single sperm cell spanning the length of a regulation tennis court (D. melanogaster sperm, by contrast, are only half their body size). Given how energetically costly such giant sperm are to produce, males adjust their production based on internal calculations of supply and demand. In one experiment by Adam Bjork and colleagues at the University of Arizona, D. bifurca males that were isolated from females produced four times fewer sperm than those who mated frequently. When mating opportunities are low, it is more efficient to shift priorities away from reproduction in order to conserve resources and vice versa. In scientific parlance, this is known as a life-history trade-off and it plays a crucial role in female sexual strategy.

There is now a growing literature, such as the recent review in Evolutionary Anthropology by Brooke Scelza, that challenges this traditional understanding of female sexual strategy to reveal a much more dynamic scenario. Darwin himself initiated this newer line of reasoning in a little quoted passage from The Descent of Man (1871): “Generally the males try to drive away or kill their rivals before they pair. It does not, however, appear that the females invariably prefer the victorious males.” Darwin further noted that many females “not only exert a choice, but in some few cases they court the male, or even fight together for his possession.” Even though it would take more than a century to do so, studies from a diversity of species have demonstrated that female sexual behavior occurs at higher frequencies than necessary to ensure conception and frequently occurs in nonconceptive forms.

For example, female cats--including leopards, lions, and pumas--are notorious for their frequency of matings. African lionesses (Panthera leo) are in estrus for a 6-7 day period during which they can mate up to 100 times a day with multiple partners. Thanks to modern genetic analysis, a recent study in the journal Molecular Ecology was able to show that nearly half of offspring in most prides were sired by extra-pair males. In the yellow-toothed wild guinea pig (Galea musteloides) promiscuous mating is driven by the female strategy of multiple paternity and results in greater offspring variability (Hohoff et al. 2003). Petrie et al. (1998) report that, until recently, 90% of all bird species were categorized as monogamous. However, in their wide ranging study of “monogamous” species, the level of extra-pair paternity ranged from 0% to 76% and was highest in populations with the most genetic variation between males. These extra-pair copulations have been demonstrated to be actively sought by the otherwise socially monogamous females (Gray 1996). In the Eurasian dotterel (Charadrius morinellus) females both compete with other females over males and choose the best potential mate to raise their chicks, the male seeming to have no role in the selection (Owens et al. 1994).

Of course, birds and mammals aren't the only class of animal where an ardent female strategy is common. The sierra dome spider (Linyphia litigiosa) engages in multiple matings that result in mixed paternity of offspring in what Watson (1991) calls “genetic bet-hedging.” Arnqvist and Nilsson (2000) report that females of the majority of insects mate with multiple males with a fitness gain of 30-70%, leading the authors to conclude that “the evolutionary maintenance of polyandry in insects can be understood solely in terms of direct effects [i.e. reproductive success].” Perhaps the most remarkable example of this comes from the yellow dung fly (Scatophaga stercoraria) in which females solicit multiple matings and retain the sperm in separate storage compartments to be actively and differentially selected following copulation (Hellriegel & Bernasconi 2000). In fact, it was this tendency for female multiple mating among the Hymenoptera that influenced E.O. Wilson to abandon the theory of kin selection (with a predictably adversarial response from Richard Dawkins, Jerry Coyne, and Steven Pinker).

The primate literature is even more dramatic and is far more important when considering the potential strategies employed by our hominin ancestors. Female saddle-back tamarins (Saguinus fuscicollis), who were once thought to be monogamous, solicit matings with multiple males, each of whom help to care for her offspring (Goldizen 1986). Mouse lemurs (Microcebus murinus) engage in “selected polyandry” by mating with between 1-7 males up to 11 times during their single night of receptivity, resulting in mixed paternity of offspring (Eberle & Kappeler 2004). Marmosets (Callithrix kuhlii) form polyandrous mating groups with no evidence of breeding monopolies by specific males (Schaffner 2004). Among barbary macaques (Macaca sylvanus) the females are reported to seek copulations with up to 10 males per day during estrus (Taub 1980) while Perry and Manson (1995) report that adolescent rhesus macaques (Macaca mulatta) vigorously court males as a strategy to compensate for low attraction in comparison to adult females. Manson et al. (1997) found that among a group of 21 capuchin monkeys (Cebus capucinus) nine of fifteen copulations between adult males and adult females occurred when females were pregnant. And, of course, female chimpanzees (Pan troglodytes) and bonobos (Pan paniscus), with whom we share some 98.6% of our DNA, are the most promiscuous of primates (Parish & de Waal 2000).

An ardent female strategy has significant impacts on the very structure of primate society. Manson et al. (1997) also demonstrated that most female capuchin monkeys sexually solicited the recent immigrant males, even when pregnant, and were more aggressive toward them after mating than with the resident males (in many cases soliciting the inter-group copulation only to chase the immigrant male away afterwards). As Sarah Hrdy wrote in her 1977 book The Langurs of Abu, in her ten year study of Hanuman langurs (Semnopithecus entellus) she found at least three different sets of circumstances under which female langurs solicit males other than their so-called harem-leaders: first, when males from nomadic all-male bands temporarily join a breeding troop; second, when females leave their natal troops to travel temporarily with all-male bands and mate with males there; and third, when a female for reasons unknown to anyone, simply develops an interest in the resident male of a neighboring troop.

This trend for inter-group pairs is significant because it has been assumed, both among human and non-human primates, that the observed social unit and the reproductive unit were identical. This led to the reasoning that male philopatry--staying in the community you were born in--resulted directly from the male reproductive strategy of “forging alliances with locally available males (usually kin) to patrol access to females in a community, protecting these females and their offspring from males in neighboring communities” (Silk 1983). However, female strategies seeking out genetic diversity among foreign mates may in fact be the defining social principle with patrilocality, dominance hierarchies, and mate guarding the male counterstrategy to increase the likelihood of paternity. In a similar vein, the prevalence of male sperm competition would be unlikely to evolve without the selection pressure resulting from such female promiscuity (Yasui 1998). This perspective has enhanced importance considering that Pan paniscus, Pan troglodytes and Homo sapiens all share male philopatry and large relative testis size (a strong predictor of sperm competition) leading to the possibility that our common ancestor likewise shared these traits.

Following this logic Kingan et al. (2003) and Dorus et al. (2004) analyzed the seminal protein DNA at both SEMG1 and SEMG2 loci respectively (genes central to semen coagulation, or ‘mating plugs,’ and which indicate positive selection for male sperm competition). Both authors found a direct correlation between levels of polyandry and selection for seminal coagulating proteins. Dorus et al. (2004) summed up the research by concluding, “the rate of evolution correlates tightly with both the level of polyandry and reproductive physiologies such as testis size and semen coagulation rating." And in both studies human semenogelin genes lie closest to chimpanzees and bonobos, suggesting that our common ancestors were polyandrous females and sperm competing males. Does this mean that humans evolved in polyamorous, or multimale-multifemale, mating groups like our closest relatives as Ryan and Jethá (2010) argue? Possibly. What is certainly clear is that human females did not evolve a one-size-fits-all strategy, but rather shift that strategy based on the environmental context.

With the Achaeans at the doorstep of Troy, Helen prostrated herself before her new father-in-law and mourned her fate. “Would that I had chosen death rather than to have come here with your son, far from my bridal chamber, my friends, my darling daughter, and all the companions of my girlhood. But it was not to be, and my lot is one of tears and sorrow.” However, Helen’s lament is not the cry supported among many females in the natural world, particularly our primate relatives. Female strategy has long involved the ardent pursuit of multiple males in order to maximize reproductive success. In effect, whether the focus is on bonobos or guinea pigs, the epic tale of Helen’s fateful choice is at this moment being reenacted in the forests surrounding the Congo river and within the burrows of South America.

The views expressed are those of the author and are not necessarily those of Scientific American.

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