How we do it: Maybe monogamy isn't natural!

From incest to sperm competition and polyamory, anatomy -- not social arrangements -- explain how a species mates

Published June 15, 2013 5:00PM (EDT)

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Excerpted from "How We Do It: The Evolution and Future of Human Reproduction"

It is tempting to assume that mating arrangements directly match the typical social pattern. For instance, in a pair-living species it might seem obvious that the adult male sires any offspring of the pair. In other words, pair-living social organization and strictly monogamous mating may appear to be two sides of the same coin. Take, for example, the thousands of pair-living bird species that have traditionally been regarded as strictly monogamous. Countless hours of observation by dedicated bird-watchers failed to reveal any deviation from strict limitation of mating to the partners in a pair. However, the advent of DNA-based paternity tests changed all that. Surprisingly, for nine out of every ten bird species studied, it was discovered that the pair male did not consistently sire all offspring in a nest; about half of them resulted from extrapair copulations. How, we may ask, did such extrapair mating escape detection through the binoculars of all those eager bird-watchers? The answer is that “sneaky” copulations are rapid and discreet. The pair male may be as unaware of them as the peeping ornithologist.

Theorists have leapt in to explain these exciting new findings, incautiously borrowing loaded terms from the human arena. Ironically, the Middle English “cuckold,” used to describe human infidelity, was originally derived from an old French word for cuckoo. Coming full circle, it is now widely applied to animals to refer to pair-living males tending offspring that may not be their own. The customary explanation for this occurrence is that it is in a female’s genetic interest for different males to father her offspring. She may pair up with one male to ensure paternal care while also engaging in extrapair copulations that will boost genetic variability in her offspring. It is in a female’s interest to conceal from her pair mate any sneaky copulations with other males. If the female’s partner were to become aware of the threat to paternity, he might abandon the nest. Or so the argument goes.

This explanation assumes that a male’s overriding interest is to strive for exclusive paternity of any offspring in his nest. Hence strong selection would be expected for any mechanism that reduces the likelihood of extra-pair copulation. Yet chances are that any pair-living male will himself seek mating opportunities with females of nearby pairs. As is the case for females, it is surely in a male’s genetic interest to father offspring in nests of females paired with other males. Perhaps there is a trade-off between a male’s interest in defending paternity of offspring in his own nest and benefits from contributing to paternity of offspring in other nests. Males, too, can spread their options. In any event, the mating arrangements of pair-living birds have turned out to be considerably more tangled than originally believed.

Thus patterns of social organization and mating systems are not simply two sides of the same coin; they can vary independently, at least to some extent. This variation also applies to mammals, including primates. DNA-based tests have been used to assess paternity in a few mammal species, and similar results have emerged. Compared to the wide array of studies conducted with birds, there have been few genetic studies of paternity in pair-living mammals, but evidence for frequent extrapair copulations will doubtless emerge. To take one example, in 2007 behavioral biologist Jason Munshi-South conducted a DNA-based study of a pair-living treeshrew species in Sabah (Borneo) and found a high level of extrapair paternity. Similar evidence has also been reported for certain pair-living primates—for example, for fork-crowned lemurs and fat-tailed dwarf lemurs, both night-active inhabitants of Madagascar. Even gibbons, the prime example of monogamy in primates, have been observed engaging in sneaky extrapair matings in the wild.

Social patterns and mating systems can differ sharply in primates. Verreaux’s sifaka, a day-active Madagascar lemur, typically lives in small, multimale groups containing about half a dozen adults of both sexes, although the male-to-female ratio varies greatly. As in most other lemurs, mating in Verreaux’s sifakas is strictly seasonal, confined to a few weeks each year. Pioneering fieldwork by biological anthropologist Alison Richard revealed that the mating season is a time of turmoil. Confirming earlier anecdotal accounts, she found that severe fighting often erupted during the mating season. Moreover, she observed that mating typically occurred between groups rather than within them. Reorganization of social groups often ensued. Thus group structure does not dictate mating arrangements and evidently has other functions. Indeed, primate field studies indicate that social organization is generally linked to feeding. So while Verreaux’s sifakas live in stable feeding groups for most of the year, those groups are disrupted by seasonal mating.

The distinction between social organization and mating arrangements also applies to humans. Extramarital sex certainly occurs, although not as frequently as media depictions or faulty statistics would have us believe. Various surveys of long-term partners, including a 2004 survey by biologist Leigh Simmons of four hundred students of both sexes, have revealed that one in four will engage in extrapair copulation at some time. The good news is that three-quarters of couples remain faithful over the long term. Moreover, the reported average rate of extrapair paternity is only around 2 percent—a conclusion confirmed by Alan Dixson in his 2009 book Sexual Selection and the Origins of Human Mating Systems. In other words, in humans a relatively low frequency of extrapair copulation results in an even lower level of extrapair paternity. Although some studies have reported a level of extrapair paternity as high as 12 percent, this seems to be exceptional. We can forget those apocryphal stories of “unpublishable” genetic studies in disadvantaged urban communities revealing that half the children had not been sired by their supposed fathers. In fact, humans in the societies surveyed seem to be more consistently monogamous than most bird species that have been studied.

Strangely, people cherish two incompatible ideas: that monogamy is the standard arrangement for human mating, and that men are less faithful than women. The original version of the doggerel quoted above, reportedly penned by Mrs. Amos Pinchot on awakening from a dream, was: “Hogamus, higamus, men are polygamous; higamus, hogamus, women monogamous.” In a similar vein, American journalist H. L. Mencken once acidly remarked: “The only really happy folk are married women and single men.” But this notion presents us with a problem: If women are typically monogamous, where do polygamous men find their extra partners? This enigma is highlighted by the finding, reported in many surveys, that men have more sexual partners than women. If, say, men report an average of ten sexual partners and women report only four, who are the six extra female partners reported by each man? One common explanation has been that, despite the promised anonymity of surveys, bravado drives men to overreport numbers of partners, while modesty drives women to underreport. Basic mathematics tells us that in a monogamous society there are only two possibilities: Either women and men are unfaithful in equal numbers, or a limited number of very promiscuous women must cater to the demands of many unfaithful men. As it turns out, a recent study revealed that prostitutes account for the inflated numbers of female partners. Apparently most men are too coy to admit that they paid for the extra experience.

Which brings us to a fundamental evolutionary question: Are humans biologically adapted for a particular pattern of social organization and mating? Cross-cultural evidence indicates that, as a species, we are highly variable in both respects. Evidence from comparisons with nonhuman primates is equally inconclusive. Despite this ambiguity, many authors resort to a shortcut. They simply take the chimpanzee as a frozen ancestor for human origins, concluding that our evolution began with promiscuous, multimale groups. At the other extreme, it is reasonable to argue that available evidence is so weak that we really cannot reach any firm conclusion regarding our ancestry. Indeed, many would conclude that there is no biological basis whatsoever for human social organization or mating arrangements and that social convention governs everything. According to this view, monogamous marriage is a purely social construct free of any biological predisposition. It turns out that both extreme views are untenable.

Differences in adult body size between males and females provide one important clue to social organization. In some primate species, males and females are almost equal in size (monomorphic), whereas in others they are significantly different (dimorphic), usually with males being bigger than females. Crucially, pair-living primate species are typically monomorphic. Males and females are approximately the same size, with an average difference below 15 percent. In harem-living and multimale species, by contrast, sexual dimorphism is common, although its extent varies widely. In extreme cases, such as African mandrills, males weigh more than twice as much as females. Humans are mildly sexually dimorphic. Worldwide averages indicate that men typically weigh just over 20 percent more than women. The actual degree of sexual dimorphism is really somewhat greater, because fat deposits account for a distinctly larger proportion of body weight in women. In prime adults, fat makes up about a quarter of body weight in women but only a tenth in men. This marked sex difference in body fat is unique among primates. Over and above this, men and women differ greatly in appearance because the fat is differently distributed. This sexual dimorphism in body size and shape provides a clue that humans are not biologically adapted to live in pair-based groups.

No discussion of human mating arrangements can gloss over the topic of incest. Incest is commonly defined as mating with close relatives, although a book review in Nature more pithily called it “multiplying without going forth.” The key point is that mating between close relatives is likely to be detrimental because of inbreeding. All human societies have some kind of incest taboo, but the specific kinds of relatives excluded differ from society to society. Unions between parents and children or among siblings are usually prohibited as a matter of course, but uncles, aunts, and especially cousins may be viewed as acceptable partners depending on the culture. Regarding marriage between first cousins, for instance, the classical Greek and Roman worlds parted company. Athens and Sparta raised no obstacle, while Rome was vehemently opposed. As a Protestant, Charles Darwin was able to marry his first cousin Emma Wedgwood without the special dispensation traditionally required for Roman Catholics, although he later worried about the dangers of marriage between close relatives.

Eminent thinkers such as Sigmund Freud and Claude Lévi-Strauss fostered a myth that incest taboos are a purely cultural construct, unique to humans. They supposed that other animals mate indiscriminately, while humans uniquely benefit from a socially prescribed taboo. However, the notion of indiscriminate mating in other animals is simply wrong. Inbreeding increases the expression of otherwise rare genetic conditions that are often harmful, so we can confidently expect natural selection to favor mechanisms that curtail mating between closely related individuals. And it does. Among mammals, inbreeding is mainly avoided through the mechanism of individuals dispersing from their place of birth. This works best if only one sex migrates; if both males and females migrate, it is possible for related individuals to end up together again. The general rule for mammals is that males migrate and females stay put, matching the expectation that individuals of the sex that invests least in offspring should move out. One outcome is that females within a group are often related, forming its social backbone.

In mammals, including primates, females clearly invest most in offspring and generally do not leave their family group. Many night-active primates show this pattern, and so do various monkeys and apes, including macaques, plains baboons, and black-and-white colobus. Long-term field studies eventually revealed a reverse pattern in some monkeys and apes, including chimpanzees, red colobus monkeys, and spider monkeys, in which males stay put and females migrate. There is no convincing explanation for these exceptions, but the result is that males, not females, form the backbones of social groups. The net effect—the avoidance of inbreeding—is the same. With pair-living primates things work differently. Here, both males and females must leave the area of birth as adulthood approaches. Thus related individuals migrating out of one group might possibly meet up in another. This occurrence can be prevented if migrating siblings avoid one another or if males, for instance, are programmed to migrate farther than females. Both mechanisms probably operate in practice.

Interestingly, in human societies it is typical for women to marry out and for men to stay put; some regard female dispersal as a human cultural universal. This surely overstates the case, but ingenious genetic analyses have confirmed that men tended to stay home far more than women during the evolution of our species. This finding is important for two reasons. First, female dispersal should reduce inbreeding. Second, evidence from non-human primates indicates that a pronounced bias toward female migration is unlikely in a species biologically adapted for monogamy.

Avoidance of inbreeding is certainly not unique to humans. But explicit incest taboos that vary from one society to another are. Why do we need them? Undoubtedly, we descended from ancestors with natural mechanisms that precluded mating between close relatives. Is it at all likely that those mechanisms disappeared early in human evolution only to be replaced by incest taboos? Rather than replacing natural mechanisms for inbreeding avoidance, incest taboos serve to strengthen them. For instance, if early humans, for some reason, were less able to disperse to avoid inbreeding, perhaps an additional aid was needed to block mating between close relatives. One simple possibility is that males and females that grow up together find each other unattractive as mates. There is evidence for such a “kibbutz effect” in humans. As far as mating is concerned, familiarity does breed contempt. Social reinforcement of inbreeding avoidance may have been needed because social organization and mating arrangements became far more flexible in humans than in other primates. With that said, we can now return to exploration of the biological basis for human mating patterns.

In examining mating patterns, we have to consider the possibility that sperms from different males may have to compete. In this respect, primate groups containing a single adult male (pairs or harems) differ fundamentally from those with several adult males. In a one-male group, the resident adult male faces no direct competition when mating. In a multi-male group, by contrast, mating is typically promiscuous to some degree, making direct competition between males and their sperms likely. There is, of course, a caveat: If females in one-male groups engage in sneaky matings with extragroup males, then there will be some competition between males. For the sake of argument, however, let us accept the idea that direct competition between males is unimportant in single-male groups but prevalent and perhaps even fierce in multimale groups, where adult males try to exclude one another from mating with resident females. Often adult males form a relatively stable dominance hierarchy, established and maintained by competitive encounters. It is generally accepted that high-ranking males will have easier mating access to females. Nevertheless, two or more males may copulate with a female during a single ovarian cycle.

This brings us to the topic of sperm competition, which opens up new avenues of thought about whether humans are biologically adapted for a particular mating system. The underlying reasoning is quite simple. Active testes are expensive organs, using about as much energy as a chunk of brain of the same size. (Indeed, a feminist friend dismissively calls the testis the “male brain.” This is not entirely without precedent. Leonardo da Vinci’s famous drawing The Copulation shows an imaginary duct connecting a man’s brain directly to his penis.) Because of their high energy demand, natural selection constrains testes to be just big enough to serve their function. When males live in multimale groups, natural selection should favor increased sperm production to boost the chances of mating success, and so males can be expected to have relatively large testes. By contrast, males living in one-male groups have little exposure to sperm competition, so their testes should be smaller. We can test these predictions with comparisons between species, although it is important to scale to body size. Other things being equal, males of larger-bodied species are likely to have bigger testes anyway, and this must be taken into account.

Zoologists Alan Dixson and Alexander Harcourt, among others, have conducted several broad-based studies of testis size in primates and other mammals. Their results have confirmed the predicted relationship of testis size with mating system. In monkeys and apes, for example, species living in multimale groups—such as macaques, baboons, and chimpanzees—all have large testes relative to body size. By contrast, males living in one-male groups typically have relatively small testes. This rule applies not only to pair-living species such as woolly lemurs, marmosets, owl monkeys, and gibbons but also to primates living in harem groups, such as various leaf monkeys and gorillas.

Human testes are relatively small. Men certainly have far smaller testes than chimpanzees, despite our larger body size. Whereas a human testis is about the size of a walnut, a chimpanzee testis is as big as a large chicken’s egg. The small size of our testes directly conflicts with any suggestion that human social and mating systems are biologically adapted for chimpanzee-like promiscuity. Judged on size alone, human testes are seemingly adapted for a one-male mating system without sperm competition. Of course, this does not tell us whether men evolved to live in pairs, harems, or an orangutan-like dispersed system.

Several other dimensions of the reproductive tract support the evidence from relative testis size regarding biological adaptation for human mating, as Dixson demonstrates. For instance, the vas deferens—the duct that conveys sperms from the testis—is shorter and more muscular in primate species living in multimale mating groups, which are subject to sperm competition. In men, by contrast, the duct is quite long and only moderately muscular. Primates with large testes also have large seminal vesicles, indicating an enhanced capacity to produce seminal fluid. In humans, medium-sized vesicles produce about two-thirds of the seminal fluid, while the prostate gland adds the remaining third. Similar distinctions are found in female primates. For example, in species with multimale groups the oviducts are relatively long, increasing the distance that sperms must travel to fertilize the egg. Oviducts are contrastingly short in species living in one-male groups, and the relatively short oviducts of women clearly fall into this category. All evidence combined indicates that the reproductive systems of both men and women are adapted for a one-male mating context with little sperm competition.

Arguments based on testis size and other dimensions, such as seminal vesicle size or girth of the sperm-carrying duct or oviduct, may be flawed. The unstated assumption is that dimensions of the reproductive organs of any given species are genetically controlled and fixed within certain limits. Yet in seasonally breeding primate species testis size usually varies markedly across the year, so seasonal variation in testis size must be taken into account. It is also possible that— regardless of seasonal variation—testis size and other dimensions are adjusted to fit local conditions. This is suggested, for example, by minor variation in testis size between human populations. Reportedly, testes tend to be smaller in Asiatic men and larger in Europeans, particularly Scandinavians. It is not at all clear whether such variations in human testis size are genetically determined or influenced by social, nutritional, or other factors.

Alan Dixson, together with Matt Anderson, elegantly resolved the issue of environmental influence. In addition to examining overall testis size, which may be influenced by local conditions, they proceeded to examine sperms themselves. Remember that a sperm consists of a head containing the nucleus, a midpiece packed with mitochondria, and a whip-like propulsive tail. Mitochondria in the midpiece provide energy to power the tail as the sperm wriggles toward its goal. Dixson and Anderson reasoned that sperms exposed to competition might have a bigger midpiece, equivalent to a bigger fuel tank. To test this possibility they measured sperms of various primates. In this case, comparisons are straightforward because, remarkably, sperm size is not related to body size. Therefore scaling analyses are unnecessary. (Hold that thought.) Anderson and Dixson found a convincing relationship between sperm midpiece size and social organization. In multimale species such as macaques, plains baboons, and chimpanzees, the midpiece is significantly larger than in single-male species such as pair-living marmosets or gibbons and harem-living gelada baboons or gorillas. In human sperms, the midpiece is quite small, clearly falling into the range of primates living in one-male groups and well below values for species with multimale groups.

So results from measuring sperm midpiece size broadly match those obtained from comparative analyses of testis size. However, there are some important differences. For example, lesser mouse lemurs have relatively large testes, resembling the condition in primates living in multimale groups, whereas the sperm midpiece is quite small, falling into the range for primates living in one-male groups. Moreover, gorillas have notably small testes even compared to other primates living in one-male groups, whereas their sperm midpieces are among the largest for harem-living primates. It is clear that testis size and midpiece size can vary independently to some extent. Nevertheless, results for humans are quite explicit: Human males have relatively small testes and their sperms have an especially small midpiece, among the smallest recorded for any primate. There is no evidence whatsoever that human testes are biologically adapted for a mating context with pronounced sperm competition. Although environmental conditions may influence testis size, they do not affect sperm dimensions. Dimensions of sperms are quite constant in humans and are likely under tight genetic control. Therefore the sperm midpiece provides us with one of our strongest clues to biological adaptation for human mating.

Excerpted from "How We Do It: The Evolution and Future of Human Reproduction" by Robert Martin. Available from Basic Books, a member of the Perseus Books Group. Copyright ©2013. 

By Robert Martin

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