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Polyandry (One Woman, Many Men)

People are polyandrous, not just polygynous.

Although polygyny (male harem-keeping) is part of human nature, so is polyandry (female harem-keeping). Ironically, we are both polygynous and polyandrous. Part of our nature inclines us to male-oriented harems, but also — albeit more subtly — to their female-oriented equivalent.

When biologists such as myself began doing DNA fingerprinting on animals, many of us were shocked to find cases in which the social partner of even some of the most seemingly monogamous bird species was not necessarily the biological father.

And people aren’t altogether different — although for understandable reasons, the sexual adventuring of women has long been more obscured. Polyandry, unlike polygyny, has only rarely been institutionalized in human societies. Yet women, like men, are also prone to having multiple sexual partners. (This may seem obvious, but for decades biologists had assumed that female fidelity was generally the mirror-image opposite of predictable male randyness.)

Male-male competition and male-based harem-keeping (polygyny) is overt, readily apparent, and carries with it a degree of male-male sexual intolerance which also applies to polyandry, whereby “unfaithful” women along with their paramours are liable to be severely punished if discovered. This intolerance is easy enough to understand since the evolutionary success (the “fitness”) of a male is greatly threatened by any extracurricular sexual activity by “his” mate. If she were inseminated by someone else, the result is a payoff for the lover and a fitness decrement for the cuckolded male.

As a result, selection has not only favored a male tendency to accumulate as many females as possible (polygyny), but also an especially high level of sexual jealousy on the part of males generally and of men in particular. This, in turn, pressures polyandry into a degree of secrecy not characteristic of polygyny. Another way of looking at it: Patriarchy pushes polyandry underground, but does not eliminate it.

Female harem-keeping — polyandry — goes against some aspects of human and mammalian biology, once again because of the difference between sperm-making (what males do) and egg-making (a female monopoly). Although a male’s fitness is enhanced with every female added to his mating prospects, it's much less true for the fitness of a female who mates with additional males. There can indeed be a payoff to females who refrain from sexual exclusivity (actually, there are many such payoffs); however, there are also substantial costs, not least running afoul of the male sexual jealousy just described.

Thus, even though females can sometimes enhance their fitness by mating with additional males, they are simultaneously selected to be surreptitious about their sexual adventuring. Hence, polyandry — unlike its overt counterpart, polygyny — is more likely to be covert and hardly ever proclaimed or institutionalized. It also doesn’t reveal itself in such blindingly obvious traits as sexual dimorphism in physical size, aggressiveness, or differences in age at sexual maturity, since unlike the situation among males, natural selection does not clearly reward such readily apparent traits among females.

Men, in their befuddlement, have had a hard time seeing female sexuality for what it is, and instead consistently either over- or under-estimate it. Thus, women have often been portrayed as either rapacious and insatiable, or as lacking sexual desire altogether.

At one time, Talmudic scholars entertained such an overblown estimate of women's sexuality (and society's responsibility to repress it) that widows were forbidden to keep male dogs as pets! But as noted psychologist Frank Beach pointed out, "any male who entertains this illusion [that women are sexually insatiable] must be a very old man with a short memory or a very young one due for a bitter disappointment." Or, as anthropologist Donald Symons put it, "The sexually insatiable woman is to be found primarily, if not exclusively, in the ideology of feminism, the hopes of boys, and the fears of men."

In this regard, it is worth mentioning that some anthropologists have recently begun reassessing the received wisdom as to polyandry’s rarity. Don’t get the wrong idea: it is still extremely unusual, although a new category, “informal polyandry,” has been proposed to include societies in which more than one man mates regularly with the same woman. These circumstances are found in a number of societies beyond the standard “classical polyandry” of the Himalayas, Marquesa Islands and parts of the Amazon basin. Informal polyandry often co-occurs with a local belief system known as “partible paternity,” in which it is thought that if multiple men (albeit rarely more than two or three) have sexual intercourse with a pregnant woman, then they literally share paternity of any offspring that result.

Granted that the evidence for human polyandry is more speculative than dispositive, here, nonetheless, is a sample of the arguments.

1. Human beings are unusual among mammals in that females conceal their ovulation. In most species, ovulation is conspicuously advertised, but not us! Indeed, even in the medically sophisticated 21st century, and despite the fact that reproduction is such a key biological process, it is remarkably difficult to ascertain when most women are ovulating.

There is considerable controversy over why women’s ovulation is kept so secret, but one intriguing possibility is that it facilitates a woman’s ability to deceive her mate as to precisely when she is fertile. If our great-great-grandmothers sported a dramatic pink cauliflower bottom when they were in season, our great-great-grandfathers could have mated with them at such times, then ignored them while pursuing their own interests. (Which notably would have included mating with other women.)

But by hiding their ovulation, our female ancestors essentially made it impossible for our male ancestors to guard them all the time, giving the option for great-great-grandma to sneak copulations with other men, of her choosing, thereby avoiding the ire of her social partner while obtaining whatever benefits such “extra-pair copulations” may have provided.

2. Women are also unusual among mammals in lacking a clear behavioral estrus (or “heat”) cycle. As a result, they are able to exert a remarkable degree of control over their choice of a mate, unlike most female mammals, who find themselves helplessly in thrall to their hormones. Absent such choice, polyandry would be indistinguishable from literal promiscuity.

The word “promiscuity” carries with it a value judgment, distinctly negative. For biologists, however, it simply means the absence of subsequent bonding between the individuals involved. Some animals appear to be truly promiscuous. For example, many marine organisms — such as barnacles, or oysters — squirt their gametes (eggs and sperm) into the water, usually responding to chemical signals but not engaging in anything like mate choice. But for the most part, promiscuity is rare, since nearly all living things — females in particular —0 are more than a little fussy when it comes to settling on a sexual partner, even as they may end up with many such partners.

Females in general and women, in particular, have a substantial interest in making a good mating choice (or choices), if only because biology mandates that such decisions are especially consequential for them, since children are born quite helpless, and their prospect of biological success is enhanced by many factors, notably parental care and attention, in addition to good genes. And indeed, females in general and women, in particular, are especially fussy when it comes to choosing their sexual partner(s).

3. Recent studies by evolutionary psychologists have shown that during their ovulatory phase, women are attracted to men whose body build and facial features reflect high testosterone and basic good health (that is, good genes), whereas otherwise, they are more influenced by indications of intelligence, kindness, sense of humor, ambition and personal responsibility. In other words, women follow a two-part reproductive strategy consistent with an evolutionary history of polyandry: mate, when possible, with partners carrying those good genes, but associate socially with those offering the prospect of being good collaborators and co-caretakers of children. For some women — those fortunate to pair with men providing both good genes and good parenting/protection prospects — the risks of polyandry (especially, their husband’s ire, potential violence and possible abandonment) outweigh the possible benefits. But for others, quite possibly the majority, the opposite can be true.

4. The adaptive significance (evolutionary payoff) of the female orgasm has long been debated. Among the possible explanations — all consistent with polyandry — is that orgasm enables women to assess the appropriateness of a short-term mating partner as a long-term prospect, while another suggests that female climax is not only rewarding for the woman in question but also reassuring for her partner, providing confidence that she will be sexually faithful … while giving her the opportunity to be exactly the opposite.

5. Given that polyandry among animals is predictably correlated with reversals in the “traditional” forms of sexual dimorphism, why hasn’t human polyandry resulted in women being larger and more aggressive than men? For one thing, it isn’t possible for men to be larger than women (which, as we’ve seen is mostly a result of polygyny) and for women to be larger than men (because of polyandry)! And for another, because of the difference between sperm and eggs, the reproductive payoff to polygyny — and its associated male-male competition — is substantially greater than that of polyandry, which in turn has caused polygyny to be the more prominent driver of human sexual evolution. This is not to claim that polygyny (acting mostly on males) is any more real than is polyandry (acting mostly on women), but rather that its effects are more dramatic and more readily identified.

6. Because of the negative fitness consequences for men resulting from polyandry on the part of “their” women, we can expect that men would have been selected to be quite intolerant of it. And indeed, sexual jealousy is a pronounced human trait — also widespread among animals — not uncommonly leading to physical violence. Such a powerful and potentially risky emotional response would not have been generated by evolution if women weren’t predisposed, at least on occasion, to behave in a way that is adaptive for them.

David P. Barash is an evolutionary biologist and professor of psychology at the University of Washington; his most recent book is Out of Eden: Surprising Consequences of Polygamy.

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