Reversal of Fortune

Where is it written in stone that the man should have all the fun? In some species of animals, evolution has made females the polygamists.

By Jared Diamond|Wednesday, April 01, 1992
RELATED TAGS: SEX & REPRODUCTION
Quick: What’s your first thought when you hear the word polygamy? Most likely it conjures up images of a sultan with a large harem--such as Morocco’s Emperor Moulay Ismail the Bloodthirsty, who sired 888 children by an uncounted number of wives. Or you might think of a nineteenth-century Mormon patriarch such as Brigham Young, who presided over nearly two dozen spouses and 47 children.

In either case you were equating polygamy with polygyny. The former word (from the Greek gamos, meaning marriage) is the general term for having multiple mates, regardless of which sex constitutes the harem. The latter word (from the Greek gyne, meaning woman, as in gynecologist) specifically refers to a man having many wives.

But if you pictured a harem of wives rather than one of husbands, you don’t have to apologize for your unreconstructed sexism: your assumption is well founded in biological reality. Among birds and mammals, polygamy usually does involve males reigning over large harems of females. Elephant seals, elk, and birds of paradise are among the polygynous potentates most familiar to us from television specials. Among humans also, most hunter-gatherer societies permitted polygyny in theory, even though in practice few men achieved it.

A simple, well-understood evolutionary reason lies behind this cruel asymmetry: in most animal species, females make a much bigger investment of time and energy in reproduction than males do. A male who discharges sperm into a female at one moment is available a short while later to discharge more sperm into another female and thereby to pass on his genes to more offspring. The female, though, must nourish the fertilized embryos until birth, and in the case of mammals, must nurse the young for some time thereafter. During that whole period a second mating would not serve to increase her genetic output. Thus in an evolutionary sense, polygamy usually pays for men but not for women.

Nevertheless, a small number of bird and mammal species, as well as various fish, amphibians, and insects, manage to break this rule. Instead of polygyny these animals practice polyandry (from the Greek andros, meaning man), in which one female enjoys the use of multiple males. Nor is polyandry limited to animals; there are even a few polyandrous human societies.

On the face of it, these rare cases are puzzling. Since one husband can fertilize as many eggs as can two, what good are extra husbands? Furthermore, what on earth would induce a self-respecting male to join a harem?

It turns out that a number of evolutionary preconditions have to be met for polyandry to occur, which is why it is rare. But that it occurs at all sheds an interesting light on sexual conflicts of interest among animals. In particular, the existence of polyandry shows there’s nothing inevitable about males getting the most sexual opportunities.

Let’s start with an extreme example of polyandry: that practiced by jacanas. In the United States these birds are confined to southern Texas as occasional visitors, but in the tropics they’re wide spread. Jacanas frequent ponds covered with lily pads, which they walk across by spreading their weight over very long toes and toenails (they are also known as lily- trotters).

A female jacana may have up to six mates simultaneously. The males do all the work of building the nests, incubating the eggs for nearly a month until they hatch, and caring for the young for two months after that. Females, meanwhile, which outweigh the males by as much as 75 percent, fight fiercely with one another for territories. Within their territories, each male sits on his own nest in his own little subterritory. Since he is so much smaller, he is rarely able to drive off an intruding female. Instead he screams loudly for his mate to defend his share of her real estate. Should a new female defeat and expel his mate, he may go through the motions of attacking the intruder. But within a few hours he accepts the inevitable and begins copulating with her.

The female jacana is in effect a big, fierce egg-laying machine. She can lay a complete clutch of four eggs as often as every ten days. But the male, as soon as he receives a clutch, is tied up with parental responsibilities for three months, during which he is incapable of accepting a second clutch. The female’s ability to make use of her enormous egg-laying potential is therefore limited chiefly by her access to males and thus by her ability to duke it out with other females. Females that lose a fight miss a chance to pass on their genes.

Female jacanas attack not only rival females but also their rivals’ eggs and chicks. A team of ornithologists from Cornell confirmed this bloody truth by removing two harem-owning females from their territories just before sunset. Within an hour of dawn a neighboring female had taken over one of the vacated territories, while two more neighbors were fighting for possession of the other. The conquerors proceeded to hunt down and viciously attack most of the departed females’ chicks, brushing aside any resistance offered by the overmatched little fathers. Within two days the murderers began to mate with the bereaved fathers.

In short, female jacanas behave like males of many other species, and male jacanas behave like females. For the successful female it’s an evolutionary dream come true: she gets to pass on her genes to far more clutches of young than she could rear unassisted. As long as she can find males willing to take over parental care, she can exploit her egg-laying potential to the fullest. As for infanticide, it brings the same benefits to a female jacana as it does to male lions and gorillas, which also kill their rivals’ young. The other sex, thus relieved of preexisting parental responsibilities, becomes available to rear the killer’s offspring.

For the male jacana the picture is somewhat mixed. Each male rears only one brood a year. What’s more, although each may believe that the brood he rears is the brood he fathered, that’s not necessarily the case. The Cornell team found by DNA fingerprinting that many jacana broods are of mixed parentage, consisting of some eggs sired by the brooding male and other eggs sired by another male of the same harem.
The near-complete reversal of sex roles among jacanas--not quite complete, because the female still lays the eggs--is an example of what is called classical polyandry, in which a female breeds individually with many males. Jacanas are not the only birds to practice it. Other shorebirds, such as some species of phalaropes and sandpipers, are polyandrous as well. But few other birds besides shorebirds practice classical polyandry, and even among shorebirds it is disproportionately frequent among species that live in tropical or mild temperate climates. These facts provide a clue to how the strange behavior evolved.

The first thing to remark about the reproductive biology of shorebirds is that they nest on the ground. As a result their young are terribly vulnerable to predators, and so the chicks’ survival chances are improved by being able to run as soon as they hatch. Shorebird young are precocial, meaning that they hatch already covered with down, with their eyes open, and able to run and find food for themselves. The parent doesn’t have to feed the chicks, just protect them and keep them warm. This gives the chicks a better chance of survival, but it also means that the job of caring for the young can be handled by a single parent. Uniparental care is a prerequisite for polygamy, whether of the polyandrous or polygynous variety.

Most mammals and many birds besides jacanas practice uniparental care. Among mammals the single parent is always the female because only she can produce milk. Among uniparental birds such as turkeys and hummingbirds, the single parent is also usually the female, simply because she has a bigger investment in the chick--an egg at hatching is much bigger and more costly to produce than semen. But uniparental shorebirds are unusual even among uniparental birds in that the single parent is the father.

The reason, essentially, is that egg-laying takes so much energy out of a female shorebird that it makes sense--even from the male’s point of view--for her to concentrate on that activity. A chick that can run around as soon as it hatches must undergo more development inside the egg than the usual helpless chick. That generally requires a relatively large egg. Now another quirk of shorebird biology comes into play: they typically lay a clutch of four of these large eggs. To accommodate four huge eggs, even monogamous shorebird females have evolved to be slightly larger than their mates. But the effort is still exhausting. In spotted sandpipers, for example, each egg weighs fully one-fifth of its mother, and the whole four- egg clutch weighs an astonishing 80 percent of her weight.

Yet the female must be capable of laying another clutch if necessary. Even with precocial young, shorebirds suffer horrendous losses of eggs and chicks. One population of spotted sandpipers studied in Minnesota in 1975 produced 157 eggs but not one fledgling; 87 of those eggs were eaten by a single mink. Likewise a study of jacanas in Guyana found that 44 out of 52 nests failed during one breeding season.

In the face of these constraints, shorebirds have evolved an understanding. The male takes over the not-too-onerous responsibility of rearing the precocial chicks alone, thereby leaving his mate free to desert the brood and fatten herself up again. The short-term advantage for the male is that his mate thereby becomes capable of producing another clutch of eggs for him quickly, in case the first clutch is destroyed by a predator. The long-term advantage is that if she does not become exhausted in one breeding season, she is more likely to survive to the next, when he can mate with her again. As with human couples, experienced bird couples that have worked out a harmonious relationship fare better at raising young than newlyweds.

But there’s a downside to the male’s generosity. His interests and those of his mate are not necessarily the same: she is trying to maximize the transmission of her own genes, as he is his. Once he assumes sole parental responsibility, the road is clear for her to use her free time in whatever way she chooses. Perhaps she’ll choose to remain available to her mate, on the chance that her first clutch might get destroyed and he might require a replacement clutch. But she also might choose to seek out some other male that’s immediately available to receive her second clutch. If her first clutch survives, her polyandrous strategy has doubled her genetic output. In the long term she can do even better--assuming she shows some restraint and doesn’t die young from exhaustion.

Naturally, other females will have the same idea, and all of them will find themselves in competition for a dwindling supply of males. As the breeding season progresses, most males become tied up with their first clutch and unable to accept further parental responsibilities. Although the number of adult males and females may be equal, the ratio of sexually available females to males rises to as high as 7 to 1 among breeding spotted sandpipers and Wilson’s phalaropes. Those cruel numbers are what drives sex-role reversal even further toward the jacana extreme in classically polyandrous shorebirds. Though females already had to be slightly larger than males in order to produce large eggs, they evolve to become still larger in order to win the fights with other females--and to dominate the males. The female further reduces her parental efforts, and woos the male rather than vice versa.

That is how monogamy may have evolved into polyandry in shorebirds--as a result of their ground-nesting habits, their huge losses from predation, their precocial young, and their clutches of few, but large, eggs. These distinctive features of shorebird biology seem to have been prerequisites for classical polyandry, but they are not sufficient conditions. Most of the 200 or so species of shorebirds don’t practice polyandry. A major reason is that most shorebirds live at high latitudes, where the very short breeding season leaves no time for a second clutch to be reared--and thus no opportunity for polyandry. Only among the minority of species that live in tropical or temperate climes, such as the jacanas, is classical polyandry easier to bring off.

Other animals besides shorebirds practice polyandry, although not of the classical variety. There is another kind, called cooperative polyandry, illustrated by a Peruvian monkey called the saddleback tamarin. Along with about 20 other species of tamarins and marmosets, it’s among the world’s smallest monkeys, weighing barely a pound.

Saddleback tamarins live in groups consisting of adults, their offspring from previous years, and the current infants. The most common adult combination is a polyandrous trio of one female and two males that share her nearly equally. Since the female is constantly receptive and shows no discernible signs of estrus, her males mate with her anytime, even when she is pregnant or lactating. It’s only because we humans behave the same way that we don’t realize how bizarre a tamarin’s sex life is by the standards of most other mammals; copulating when a female is infertile makes sex a huge waste of time and effort, and it therefore demands a scientific explanation. That explanation, it turns out, is intimately connected with the animals’ polyandrous behavior.

There are two compelling reasons why tamarins are so perverse as to choose polyandry. One is that, as the smallest monkeys, they are at risk from a whole army of predators, ranging from eagles to snakes to ocelots. Wild saddleback tamarins appear constantly scared and watchful. When a tamarin group is feeding, one member of the group is always on full-time sentinel duty. For a tamarin to attempt single parenthood would constitute suicide. Even biparental care wouldn’t work, because one parent would be forced to eat and carry the infant at the same time--not an easy task for a small monkey.

The need for polyandry is made even more desperate for another reason, dear to my heart. To make up for all the young they lose to predators, tamarins regularly give birth to twins. (Being two-breasted primates, they can’t afford bigger litters.) As the father of twin primates named Max and Joshua, and having just wrenched my back carrying my progeny around my house, I know what that means. At birth, each twin tamarin already weighs one-tenth of its mother--as if my wife had given birth to two 13-pound babies. By the time they’re weaned, the tamarin twins’ combined weight is nearly half of the mother’s. Yet tamarins live in trees, making it necessary for the twins to be carried constantly while they’re small. Even one infant is a significant burden, such that the monkey carrying it is rarely able to feed or forage.
The nursing mother can’t do much of the carrying, because she has to eat double her usual amount to produce enough milk. In addition, remember that there should always be one tamarin in each feeding group on sentinel duty, not eating. As a result, even a father and mother together wouldn’t be enough to take care of the twins. The couple has no choice but to admit another tamarin to the group, and that usually means an adult male, because an adult female would probably produce more twins and compound the problem. Both males spend more time carrying the infants than does the mother. Even the older offspring help with carrying.

But the second male isn’t going to be a full-time baby-sitter for nothing. That’s why both males get equal sexual rights, making the system a cooperative polyandrous one rather than a couple with a friend. That’s also why the female is always sexually receptive, to provide both males with regular inducements. She conceals signs of ovulation in order to string them along: neither male knows when she is fertile, neither is sure who the father is, and both think, That might be my kid.

And each male profits from the other’s presence. Yes, each sires on the average only half the offspring, but a monogamous male would have difficulty rearing any offspring at all. Even the older offspring benefit from being baby-sitters. The survival of their siblings promotes the survival of their own genes. They also gain valuable child-care experience, without which both male and female tamarins have poor child-rearing success as adult parents.

From my own perspective as a father of twins, I can understand the tamarin solution. I too can’t shop or eat while carrying Max and Joshua on my back. Granted, my wife and I have found a different solution: a twin stroller, plus an adult female housekeeper whose reproductive career takes place outside our house. While we haven’t had to resort to cooperative polyandry, I still appreciate--particularly at those desperate moments when I’m feeling most overwhelmed by my twins--why it makes good sense for a monkey father without a stroller or housekeeper. As it happens, some human societies do practice polyandry, but as we’ll see, for completely different reasons.

There are many reasons for polyandry, in fact, and many other variations on the basic behavior pattern. The Galápagos hawk practices cooperative polyandry in a particularly aggressive way. Lucky females each co-own a territory with as many as five unrelated males, all of whom mate equally frequently with her, hunt food for her young, and defend the territory. While females compete individually for territories, the males compete in coalitions. The losers of both battles are in effect rendered homeless, with little prospect of breeding. The ultimate reason for this unseemly behavior is that the Galápagos aren’t such a great place to live for a hawk. Food is too scarce to support a large population of hawks, and there’s no nearby place to which to immigrate. A monogamous male has difficulty feeding his chicks and driving off coalitions of rival males. Through polyandry, males can at least make the best of a bad deal.

A chickenlike flightless bird called the Tasmanian native hen practices a similar cooperative polyandry, except that the wife-sharing males are usually brothers. That reduces the genetic disadvantage of polyandry to each male: if you’re not the lucky male that fathered the babies, at least the guy doing it was a close relative who shares many of your genes. Acorn woodpeckers also form coalitions of related males, with the difference that in certain places some coalitions mate not with a single female but with a group of sisters. That results in simultaneous polyandry and polygyny, or polygynandry.

But we can identify much more closely with yet another population, whose behavior bears resemblances to that of all these birds: a group of ethnic Tibetans in the highlands of Nepal and Tibet. Polyandry is rare among human beings, and this population is the best-studied example. Many families consist of a wife with up to five husbands, as with the Galápagos hawk. The cohusbands are usually brothers (as with Tasmanian native hens), though in some areas father and son are also acceptable. In a family with more than one son, the oldest brother marries when he comes of age. Each younger brother then later joins him as cohusband. While the oldest brother exercises authority, all brothers theoretically share equally in the wife’s affections and sexual favors.

For an individual Tibetan woman, polyandry may or may not increase the output of children. So why is it popular? The key factors-- much as in the Galápagos--are that the Tibetan plateau is a harsh, dry environment where it’s hard to make a living and that traditionally there has been no opportunity to emigrate. People live as farmers and herders on small plots of land. If parents divided their land and animals among their children, each would inherit an uneconomically small estate. Hence the main motives that Tibetans themselves give for polyandry are to avoid at all costs subdividing property and to increase the number of workers per household. While each brother might prefer a separate household, polyandry is the lesser evil.

Since polyandry takes care of more men than women, an astonishingly high proportion of adult women (31 percent, according to one study) remain unmarried in the Tibetan highlands, and no more than half of them have children. In addition, plenty of younger brothers become monks rather than settle for being junior husbands. With so many adults not reproducing, Tibetan polyandry functions as a system of birth control in an unproductive environment.

Among the fraternal cohusbands, though, all is not happiness and equal sexual rights, whatever the theoretical ideal. For example, if the oldest brother marries a 20-year-old woman when he’s 20, his 5-year-old kid brother may not be satisfied, on reaching age 20, with a sex partner 15 years his senior, even if she wanted him. Many younger brothers rebel against the elder brother’s authority and leave home to search for a job and economic independence as a springboard to monogamy.

Polyandry illustrates how biological traits that at first seem counterintuitive can be understood in evolutionary terms. It involves the familiar principles of natural selection operating on animal behavior. The outcome is exceptional only because the principles are operating under exceptional circumstances--such as the constraints imposed by shorebird biology, tamarin twins, or the Tibetan plateau.

That’s why polyandry is far more instructive than one would expect from its limited frequency. For a long time evolutionary biologists thought of natural selection as somehow promoting the good of the species. In fact natural selection operates in the first instance on individual animals and plants, and the self-interests of different individuals, even of parents and children or of fathers and mothers, may not coincide. What makes individuals of one age and sex successful may not increase the success of other classes of individuals, or may not enhance the competitive ability of their species vis-à-vis other species.

In particular, behavior that is in a man’s genetic interest may not necessarily be in the best interest of his wife, and vice versa. In most animal species, males provide no parental care and try their best to be polygynous. The male thereby advances his own genetic interests at the expense of his mates and offspring. Throughout history, human males have shown similar tendencies, although men are not as extreme in their selfish behavior as the males of most other species of mammals.

Yet clearly there’s nothing inevitable about a male-dominated world. There are also circumstances under which females have come to be bigger, fiercer, more polygamous, and less responsible as parents. Should harsh, Tibet-like conditions become more widespread on Earth--or, God save us, should twin births become more frequent--then polyandry might become the rule for humans, as it already is for certain tamarins and Tibetans.
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