In the ordinary course of events, a male dung fly copulates with a female for a full 40 minutes, and even when he is finished delivering what he came to deliver and disengages, he hangs onto her for an additional 20 minutes. Otherwise, she is likely to--how to put this?--collect sperm from another suitor. When a male ghost crab mates, his first move is to shoot into his beloved a bit of fluid that hardens into an epoxylike plug. The plug blocks any rival sperm that may have arrived earlier from swimming out of the tract where the female stores the wiggly gifts that males deposit, and so keeps the other guys' sperm from reaching her eggs. Only then does the latest crab, optimistic about his paternal chances, introduce his own sperm. The male redback spider, seconds after inseminating a female, does a somersault into her mouth so he becomes her postcoital meal; since matings followed by cannibalism last twice as long as those that don't, his ultimate sacrifice improves the chance that his own sperm will fertilize her eggs before someone else can have at her.
From behavior to physiology to anatomy, sex throughout the animal kingdom has always been and will surely always be more bizarre than the Kama Sutra lets on. But at least it's becoming less mysterious. Such previously inexplicable facts of life as weird genitalia and ludicrous copulatory practices (such as the 79 straight days that stick insects remain in flagrante delicto), biologists are now realizing, are adaptations to something they managed to overlook for a few millenniums: female promiscuity. "Generations of reproductive biologists assumed females to be sexually monogamous," says biologist Tim Birkhead of the University of Sheffield in his new book "Promiscuity," a masterly recounting of scores of recent studies. "But it is now clear that this is wrong. Females of most species... routinely copulate with several different males."
How routinely? Once they started looking, biologists found promiscuous females in some 70 percent of the species they studied. A clutch of grasshopper eggs can have several fathers. Thirty-five percent of baby indigo buntings, a pretty little songbird, are sired by a male other than the guy Mom came in with. So are 76 percent of Australian fairy wrens. In five hours, a female Scottish Soay sheep paired up with seven rams for a total of 163 encounters. Female chimps copulate a total of 500 to 1,000 times for each pregnancy: a 1997 study using DNA to run paternity tests found that 54 percent of baby chimps were fathered by males other than Mom's supposed partner. A single clutch of goshawk eggs is inseminated some 500 times. Female monogamy is the exception rather than the rule, contrary to the pat sociobiology argument that only men gain an evolutionary edge by spreading their seed widely. Surveys find that human females'--that is, women's-- "ideal number" of lifetime sexual partners is less than men's, and that they indeed have fewer partners than men. Based on that, "a lot of people want to simplify human mating and say that women are monogamous and men are promiscuous," says psychologist David Buss of the University of Texas. "But that's a gross oversimplification: both sexes pursue both strategies."
Female promiscuity triggers a war between the sexes. If a male is to have a fighting chance of fathering offspring and getting his genes into the next generation (the definition of evolutionary success) in the face of faithless females, he needs both crafty mating habits and seemingly outlandish mating equipment. One favored adaptation is a penis decked out with features much more elaborate than your basic sperm-meets-ova job requires. Hence the tools of male damselflies and dragonflies: both are covered with horns and hooks whose sole purpose, biologists have finally deduced, is to scoop out sperm that have arrived in the female's genital tract before theirs. The wild variety in testes size (relative to body size) throughout the animal kingdom suddenly makes sense in light of female promiscuity, too: the more promiscuous the females of a species, the larger the equipment a male grows so his sperm have a swimming chance at fatherhood. That's why gorillas' testes are small (faithful females) but chimps are... well, there's a reason circus chimps are usually clothed.
Scientists aren't sure what influences the females of a species (or the males, for that matter) to remain monogamous. But in humans, female promiscuity is a response to tough living conditions. In Bhutan, many women practice polyandry because in the poor valleys of the Himalayas a lone husband cannot support a family. Spouse exchange among the Inuit improves their chance of survival in the unforgiving Arctic because kin are morally obliged to provide for each other; the more in-laws, the more support.
Which brings us to the central question: what do females get out of promiscuity? (No, besides that.) One benefit of polyandry is increased resources and protection for a female and her brood. Most males are happy to trade food for sex; every male a female cricket copulates with brings her a protein-rich meal, good for her eggs. And female Adelie penguins collect a stone, to build a nest, every time they offer themselves to a male. Females also gain by sowing the seeds of confusion, paternity-wise. Each Galapagos hawk that mates with a female helps rear her chicks, even though some are not the sires. But by trading sex for paternal care, the female increases the chance that her chicks will survive. Female red-winged blackbirds who copulate with multiple males are less likely to lose their chicks to predators: each male, thinking he may be Dad, attacks would-be predators. Male primates and lions commit infanticide against babies not their own; by confusing paternity, female chimps and lionesses keep more of their offspring out of harm's way.
Female promiscuity may bring not more offspring (as male promiscuity does) but better ones. Females of several species seem to have a mysterious detector built into their reproductive system that rejects "genetically incompatible" sperm but accepts sperm whose DNA complements their egg's, producing the most viable offspring. Several studies find that females produce better-quality offspring by mating with several males; scientists are only starting to figure out how females discriminate duds from winners. Some aspects of sex, it seems, will remain a mystery. Thank goodness.