Darwin acknowledged that the pattern he’d described was sometimes reversed, with females being competitive or ornamented, and males appearing in the choosy, less spectacular style. But this was less common because, Darwin suggested, the challenge to be chosen usually fell more strongly on males than on females. He implied that this was due somehow to differences in the size and mobility of sperm versus eggs. But it was Bateman who, picking up on this idea and developing it, offered the first compelling explanation for why it is that males compete, and females then choose from among them.
The goal of his research was to test a prediction from sexual selection theory. Just like natural selection, sexual selection needs variation in reproductive success in order to work: if everyone is equally successful in producing offspring, there’s no basis on which to weed out less successful individuals. If, as Darwin suggested, sexual selection acts more strongly on males, then this implies greater variation in the reproductive success of males than in females—that is, a wider range between the least, and the most, reproductively successful individuals. Bateman put this assumption to the test for the very first time.4
To do this, he ran six series of experiments in which male and female fruit flies (Drosophila melanogaster) were trapped together in glass containers for three to four days. At the end of this period, Bateman worked out as best he could how many offspring each male and female had produced, and from how many different mates. He needed considerable ingenuity to do this, since the discipline of molecular biology, that today brings paternity-testing kits to supermarket shelves, did not exist in the 1940s.
A screen-buff might be tempted to describe the solution he came up with as a cross between Frankenstein and Big Brother. Each fly in his series was inbred with a different, distinctive mutation: some with charmingly evocative names (like “Bristle,” “Hairless,” and “Hairy-wing”); others distinctly creepier (such as the miniature- or even no-eyed “microcephalous” fly). Each fly had one dominant mutant allele (one of the two copies of a gene) and a recessive normal one: meaning, as you might distantly recall from high school biology class, roughly a quarter of the offspring would end up with a mutation from both mother and father, a quarter from the father alone, and another quarter from the mother alone. (The last lucky 25 per cent of the offspring would have no mutations at all.) This principle of genetic inheritance enabled Bateman to estimate how many offspring each male and female had produced, and how many different mates a fly had enjoyed.
The outcome of Bateman’s six series of matchmaking was the first scientific report of greater male variation in reproductive success. For example, 21 per cent of males failed to produce any off-spring, compared with only 4 per cent of females. Males also showed greater variation in the estimated number of mates. But it was the linking of the two findings that became the basis of explanations for why males compete and females choose: Bateman concluded that although male reproductive success increased with promiscuity, female reproductive success did not. His critically important explanation was the now familiar insight that male success in producing offspring is largely limited by the number of females he can inseminate, whereas a female gains nothing from further pairings beyond a single one (since her first mate should furnish her with plenty more sperm than she needs).
Interestingly, Bateman’s study was largely ignored for over twenty years.5 Then his argument was expanded in a landmark paper by the evolutionary biologist Robert Trivers.6 In this paper, the economics of egg and sperm production was made more explicit, being expressed in terms of the larger female investment of a big, costly egg compared with the male’s minuscule contribution of a tiny, single sperm. Trivers also pointed out that the lopsided costs of reproduction can go well beyond sex differences in the size of the original contribution of gametes (that is, the egg versus the sperm) to include gestation, lactation, feeding, and protection. Any female readers who have themselves reproduced will, I’m sure, be inclined to agree with this point about the substantiveness of the female mammalian reproductive role. (My own personal understanding of this deep truth occurred during my first pregnancy, on reading an unhelpfully vivid description of childbirth as a physical feat comparable to a person making their way out of a car via the exhaust pipe.) The more highly investing sex—usually females—should therefore hold out for the best possible male, Trivers speculated, as the costs of a poor-quality mating are considerable. But males would do best to compete with other males in order to spread their cheap, mass-produced seed among as many females as possible. A follow-up implication, argued Trivers, is that males usually have less to lose and more to gain from abandoning existing offspring in pursuit of a new mate.
The Bateman paradigm, as it’s sometimes known, was for a long time “the guiding principle and cornerstone for much of sexual selection theory.” As University of Missouri–St. Louis evolutionary biologist Zuleyma Tang-Martínez puts it:
Up until very recently, the unquestioned assumptions underlying the study of sexual selection have been that eggs are expensive while sperm are unlimited and cheap, that males should therefore be promiscuous while females should be very choosy and should mate with only the one best male, and that there should be greater reproductive variance among males (as compared to females) because it is males that compete for females and mate with more than one female. Since females are, presumably, mating with only one male, this means that some males may mate with many females, while others may mate with few or none. This reproductive variance is then responsible for the sexual selection of traits possessed by the more successful males.7
Indisputably elegant, Bateman’s conclusions, elaborated by Trivers, enjoyed the status of universal principles for many years. They also became the bedrock of claims about evolved differences between women and men, in which peacock tails are replaced with Maseratis, corner offices, or big shiny trophies. Just replace the phrase “many females” with “many girlfriends” and “traits possessed by the more successful males” with “Maseratis possessed by the more successful males” and the dots are all connected. From this evolutionary perspective, a woman aspiring to high status is a bit like a fish aspiring to a bicycle.
But in the past few decades there has been so much conceptual and empirical upheaval over sexual selection in evolutionary biology that, according to one professor in that field I spoke to, the classic Bateman and Trivers papers are now largely cited for sentimental reasons. And startlingly, the first set of contradictory data we’ll look at comes from Bateman’s own study.
ALTHOUGH BATEMAN’S CONCLUSIONS tend to evoke images of the Playboy Mansion or well-stocked harems, it’s necessary for the time being to return to Bateman’s unsalubrious glass containers. It was only in our young century that, noticing that this (ahem) seminal paper had never been replicated, or apparently even subjected to close inspection, the contemporary evolutionary biologists Brian Snyder and Patricia Gowaty reexamined it. As they acknowledge, they returned to the study with many advantages that Bateman had lacked. These included modern computational aids, more sophisticated statistical methods and—perhaps I can dare to add?—fifty years of feminist insights into how cultural beliefs can affect the scientific process.8 Like other modern critics of the Bateman study, Snyder and Gowaty expressed considerable admiration and respect for Bateman’s “groundbreaking” study. But as they point out, given its “foundational nature,” it was “important to know that Bateman’s data are robust, his analyses are correct and his conclusions are justified.”9 As it happens, no such reassurance was forthcoming. Snyder and Gowaty’s inspection revealed some significant problems.
For a start, as you’ll recall Bateman used different mutant Drosophila strains so that he could infer reproductive success from the particular pattern of abnormalities passed on to each offspring. If this method had you squeamishly pondering the grisliness-squared of a fly unfortunate enough to inherit both a maternal and a paternal mutation, you are one step away from a significant problem: these mutations turned out
to affect offspring viability, and Bateman only counted surviving young in his tallies.10 But if, on the other hand, a fly was more likely to survive because it had only one mutation, or none, then it could only be assigned, at best, to one parent. With the parentage of so many fertilizations completely or partially unaccounted for, this left considerable scope for error. While Bateman recognized this issue, Snyder and Gowaty quantified it. They noticed that in two-thirds of Bateman’s series of experiments, his data indicated that males had produced more offspring than the females: a logical impossibility, since every offspring of course had both a father and a mother. In other words, the data had been biased towards counting the offspring of males.11 This bias is important because the very point of the study was to compare male and female variance in reproductive success, yet the data were biased in ways likely to inflate estimates of the male variance.
Even setting aside this source of bias in Bateman’s data, a vital problem remains, raised first by Tang-Martínez and Brandt Ryder.12 While recognizing that Bateman’s study was “ingenious and elegant,”13 they also pointed out that his famous finding that only males benefit from promiscuity—immortalized into a universal principle—actually only applied to his last two series of experiments. For reasons that remain obscure,14 Bateman analysed the data from the first four series separately from the last two, and presented them in two separate graphs. Remarkably, females did show greater reproductive success with a greater number of mates in the first four series, albeit less so than males. But in the discussion section of his article Bateman focused primarily on the results that fit the notion of competitive males and choosy females. As Tang-Martínez notes, this selective focus was then perpetuated by others:
With a few exceptions, most subsequent researchers presented and relied only on the data from Bateman’s series 5 and 6 (Bateman’s second graph). General discussions of sexual selection, and even textbooks in animal behavior, almost always presented only the second graph and the discussion was limited to these results, usually as an explanation of why males are promiscuous and females coy and choosy. The results of series 1–4, and any discussion of increases in female [reproductive success] as a function of the number of males the female mated with, for all practical purposes disappeared from the literature.15
To see what the results looked like without the apparently arbitrary split among the experimental series imposed by Bateman, Snyder and Gowaty reanalysed data from all six series pooled together. As they drolly point out, if only Bateman had done so himself, he could have proudly laid claim to the first evidence of the reproductive benefits of female promiscuity! Reproductive success increased with number of mates for both females and males, and to a similar degree. Considered together with the bias towards counting fathers’ offspring, they concluded “that there is no serious statistical basis in Bateman’s data for his conclusion that the reproductive success of females does not increase with the numbers of mates females have.”16
It probably goes without saying that it is something of a setback that Bateman’s principles are contradicted by Bateman’s data. Of course, evolutionary biologists interested in sexual selection weren’t idly lolling around for decades on the grounds that good old Bateman had discovered everything they needed to know back in 1948. They were busy doing experiments, and contemporary research has identified many species to which Bateman’s principles do appear to apply.17 However, Drosophila melanogaster turn out to be just the beginning of a more complicated empirical story. By 2012, a lengthy table in an academic behavioural ecology journal listed thirty-nine species, from across the animal kingdom, in which research had established that female promiscuity brings about greater reproductive success.18 And while in many of these species this link is nonetheless stronger for males, sometimes it’s equal (for instance, in the yellow-pine chipmunk and the wild eastern salamander).19
This helps to explain why, contrary to the historical understanding that promiscuity is generally the preserve of males, it’s now clear that female promiscuity is abundant across the animal kingdom—from fruit flies20 to humpback whales21—and is “widespread” among primates.22 This revelation owes a large debt to the DNA paternity-testing techniques that have enabled researchers to part the veils of discretion that previously obscured rampant female promiscuity (most particularly in many supposedly monogamous female birds).23 Consider the lek: a mating arrangement in which males compete with each other in a specific territory or arena in a winner-takes-all conflict for sexual access to females. It is the paradigm case of competitive males and choosy females. But in some species, on closer inspection with the benefit of paternity-testing techniques, it has been turned upside down. For example, observations over two years of the buff-breasted sandpiper, a beautiful shore bird, suggested that in line with traditional expectations of how leks operate, one fortunate male was seen to be involved in 80 per cent of matings in the first year, and 100 per cent in the second.24 Well worth him taking any risk to reach that top-bird position, you would think. But DNA paternity testing of over 160 offspring hatched during that time revealed that much had taken place out of sight. Far from one or two males having all the reproductive luck, at least fifty-nine different males had fertilized eggs in the forty-seven broods tested! (Eggs from the same brood can have different fathers.) This meant that “there were actually more fathers than mothers.”25 Recall, there’s supposed to be only one father shared among the entire community of mothers. Moreover, most males only bore offspring with a single female, yet a remarkable 40 per cent of the broods had more than one father.
There could hardly be a greater contrast to traditional understanding of how a lek operates. It’s as if the women of a harem were to casually comment to the sultan when he popped by, “Oh no, that child’s not one of yours—that’s the second footman’s daughter.… Eh? Ah, sorry. He’s not yours either, that’s the son of the chauffeur. Hang on, sultan, we’ll find your kid. Nadia… Nadia! Do you remember which of these kids is the sultan’s? Oh, yes, that’s right. That boy over there playing with his half-brother. He’s yours. Almost certainly.”
In fact, there were already striking reports of female promiscuity even in the 1960s and 1970s, as University of California, Davis, behavioural ecologist Sarah Blaffer Hrdy has pointed out. Take the big cats, such as the lioness who might, during oestrous, mate as many as a hundred times a day with multiple lions. Or, consider savanna baboons, reported to actively seek numerous, brief pairings.26 Yet somehow observations such as these failed to make much of a conceptual dent: perhaps because, as Hrdy wryly suggests, “theoretically the phenomenon should not have existed.”27 (As anthropologists like to quip: “I would not have seen it if I hadn’t believed it.”)28
Hrdy can lay claim to the best-known challenge to the notion of female monogamy. While studying a gray, black-faced species of langur monkey in India as a graduate student of Harvard University, she noticed that the females would routinely solicit mates other than “their so-called harem-leaders.” As Hrdy describes her slow intellectual dawning:
My own first glimpse of a langur, the species I was to spend nearly 10 years studying intermittently, was of a female near the Great Indian Desert in Rajasthan moving rapidly through a steep granite canyon, moving away from her natal group to approach and solicit males in an all-male band. At the time, I had no context for interpreting behavior that merely seemed strange and incomprehensible to my Harvard-trained eyes. Only in time, did I come to realize that such wandering and such seemingly “wanton” behavior were recurring events in the lives of langurs.29
Given the risks and costs of these “excess” matings (such as disease and predation risks for leaving the group, as well as the investment of time and energy that could be spent doing something else), this was behaviour that required explanation. (Hrdy suggested that it helped to leave open the father’s identity, making it less likely that the mothers’ offspring would be killed.) Since this justly famous scientific revelation, researchers have come up with
all manner of ingenious suggestions as to the advantages female animals might gain from multiple mates. Since it only seems fair that women, too, should have access to evolutionarily flavoured “the-whisperings-of-my-genes-made-me-do-it” excuses for cheating on a partner, I provide a selection of these ideas here. Proposed gains of female promiscuity include genetic benefits, healthier offspring, and the opportunity to set up sperm competitions that weed out inferior specimens. It’s even been suggested that females may have sex with several males in order to sabotage the reproductive success of rivals, by depleting local sperm stocks.30
If this last possibility sounds more ludicrously Dr. Evil than Mother Nature, this may be because of how effectively the Bateman principles obscured the notion of female competition.31 For years, it was assumed that, since even the most mediocre female can achieve the very modest feat of getting herself fertilized by an eager male, every adult female will reproduce just about as well as the next. Females, then, would be under little selection pressure to develop traits that give them a reproductive edge over other females. But as Hrdy pointed out more than three decades ago, and ongoing research continues to confirm, a female’s status and situation can have major repercussions for her reproductive success—particularly over longer time periods, during which discrepancies in male reproductive success may even out somewhat, as males take turns at being “king of the hill.”32 Among primates, for instance, low-ranking females’ ovulation may be suppressed by nearby dominant females, or they may be so harassed by other females that they spontaneously abort. In the event that they do successfully give birth, their offspring are less likely to thrive and survive, thanks to inadequate food, harassment, or even infanticide at the hands of unrelated females. Gruesomely, these marauding females have even been known to eat the infants they kill. Meanwhile, in species like the chimpanzee, higher-ranking females reproduce at a faster rate, and their infants are more likely to survive, apparently due to access to richer foraging sites.33
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