Competition Is Discerned in Sperm
By NICHOLAS WADE

In the battle of the sexes, there are the formal rules -- the rich variety of variously heeded laws and customs by which each society tries to constrain reproductive behavior. 

Then there are the other rules, often in conflict with the first, which govern love and desire and the delicate games men and women play with one another. 

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If anatomy is destiny, then men can expect unfaithful mates. 

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If these other rules, the ones built into human nature, could be specified, they would not tell what is right -- that is the province of the first set of rules -- but they would help understanding of how human sexual and social behavior have evolved. 

Primatologists, who study the group of mammals that includes monkeys, apes and people, have developed some surprising ideas about the nature of the human mating system, suggesting that women may not be as faithful as their mates may suppose. And some biologists think that the deceits of the mating game may even be reflected in the hapless spermatozoon. 

People's two closest evolutionary cousins, gorillas and chimpanzees, have evolved two very different patterns of sexual behavior and social organization. 

Gorillas practice "female defense polygyny," with one male guarding a harem of females, whereas chimpanzees band together in multimale, multifemale groups. 

Behavior and anatomy, as might be expected, are closely allied. When female chimpanzees ovulate, they may mate with every unrelated male in the group, despite the dominant male's attempts to control access. One female observed by the primatologist Jane Goodall copulated with seven males 84 times in eight days. 

In these circumstances, a male's chances of paternity require the delivery of large volumes of sperm to flood out the competition, and infants are conceived after competition in the reproductive tract between sperm from rival males. Hence, chimpanzees have evolved large testicles, in relation to their body weight, and can ejaculate high sperm counts many times a day. 

Gorillas have small testicles compared with their body size, presumably because the reigning silverback can prevent his troop from being inseminated by other males; his sperm need only fertilize, not compete. 

This gorilla-chimp difference provides an interesting scale on which to try to place humans. In relation to his body size, a man's testicles are considerably smaller than a chimpanzee's, but larger than a gorilla's. 

So is sperm competition a feature of the human mating system, at least in the evolutionary past if not now? 

Men have evolved "to defend at the sperm level against their mates' having another lover in the same fertile period -- not many others, but one or two," Alison Jolly, a Princeton primatologist, wrote in her 1999 book "Lucy's Legacy" (Harvard University Press). 

Men, too, seem adapted to take more than one partner, to judge from the size difference between men and women. In the monogamous primate species, males are generally the same size as females, but this 1 to 1 size ratio increases with the degree of polygyny, reaching 1.36 to 1 in chimpanzees and 2 to 1 in gorillas and baboons. By this index, humans are not a monogamous species, because the male-female size ratio is about 1.15 to 1. 

"We conclude that human males 'expect' perhaps two or three mates," Dr. Jolly writes. 

"Mild polygyny," in her judgment, is the condition under which this size difference evolved. 

Sperm competition, if it exists in humans, would have considerable bearing on the innate rules of sexual behavior, as it would imply women were often inseminated by more than one male during their fertile period. "Sperm competition is possible in Homo sapiens, though whether it has played a significant role during human evolution remains highly debatable," Dr. Alan F. Dixson, director of the Center for the Reproduction of Endangered Species at the San Diego Zoo, wrote in his 1998 book "Primate Sexuality" (Oxford University Press). 

In a striking study, two English biologists, Dr. Mark A. Bellis and Dr. R. Robin Baker, found that men's sperm counts were higher the longer they had been separated from their partners, as if to compensate for any infidelity in their absence. Dr. Baker believes that the many malformed sperm seen in human ejaculates have a purpose -- to block or kill competing sperm. 

But others argue that human sperm is of low quality for exactly the same reason as is a gorilla's -- the general lack of competition. 

Into this academic tussle, the human genome project has inserted a remarkable new finding. Drawing on the information piling up in DNA databanks, Dr. Chung-I Wu and other geneticists at the University of Chicago reported last month that three genes related to sperm function had been evolving at a particularly rapid clip in both humans and chimpanzees, but somewhat more slowly in gorillas. A brisk rate of evolution, as reflected in the number of changes in the genes' DNA sequence, implies intense selective pressure. 

Dr. Wu noted that his finding fit neatly with the primatologists' inferences about sperm competition in chimpanzees, and its relative absence in gorillas. And his data seem to put humans in the same camp as chimpanzees. 

Not everyone is ready to buy this implication. "Humans nowadays don't look as if they have any history of sperm competition," said Dr. Richard Wrangham, a chimpanzee expert at Harvard. 

He infers that the mating system of early human groups, probably with females' having "a principal partner plus occasional others," was very different from the multimale system of chimps, with many matings on the same day. 

Dr. Alexander Harcourt, an expert on gorillas at the University of California at Davis, notes that women have evolved many means to protect the uterus from invading bacteria, and that these defenses will also harm sperm. 

It may be the sperm's need to co-evolve counterdefense mechanisms, not sperm competition, that explains the signs of evolutionary pressure seen in the DNA data, he suggests. 

One notable difference in the sexual behavior of people and chimpanzees lies in the females' ways of advertising their receptivity. 

Chimpanzees display a visible swelling during their fertile period. Women, on the other hand, evolved "enlarged breasts and buttocks, permanent advertisements to any male around," in Dr. Jolly's words, yet they concealed the time of ovulation. 

The meaning of women's concealed ovulation has attracted much speculation among primatologists. Is it a strategy to keep a favored partner around, so he can be sure of his paternity? Or a means for a woman to sleep with many men, buying protection for herself and her children by allowing each poor dupe to assume his paternity? Or perhaps both? 

Dr. Dixson, having surveyed the sexual behavior of some 200 primates in considerable detail, suspects the concealed ovulation question is being approached the wrong way around. Just as likely, he believes, unobtrusive ovulation may have been the normal state of affairs and it is the flamboyant sexual swelling among chimpanzees and baboons that needs to be explained. 

Dr. Baker, on the other hand, sees concealed ovulation and sperm competition as two sides of the same coin. To give her children the best genetic endowment, he believes, a woman should foster sperm competition and act so as to "promote sperm warfare," he wrote in his book "Sperm Wars" (BasicBooks, 1996). 

Dr. Baker's views on sperm competition, though different from those of most primatologists, rest on important biological data -- chiefly the collection of intimate secretions from many assenting couples -- that so far only he has obtained. 

The view of women as wielding considerable manipulative powers offers an interesting counterpoint to the usual descriptions of male dominance. 

"You can't pretend biology isn't there, and from many points of view, it is liberating, portraying active, entrepreneurial, ambitious females," Dr. Jolly said. 

From one society to another, men and women flaunt the property the other sex needs to assure its genes safe passage to the next generation. Men advertise their wealth and power, which women need to protect themselves and their children. 

To signal their reproductive potential, "Women use rouge to make the cheeks rosy, indicating that they have either been exercising or are sexually aroused, and lipstick to mimic the dark, blood-engorged state of the lips during sexual excitement," writes Dr. Bobbi S. Low in "Why Sex Matters" (Princeton University Press, 1999). 

Dr. Baker, a firm believer that sperm competition occurs in people, argues that women look for men to provide both resources and good genes, and the obvious strategy is to choose the best available compromise candidate as a husband. But the available choice of long-term resource-providers may be limited. So the alternative strategy for women, Dr. Baker writes, is that "they can choose the best available long-term partner, and then rely on infidelity to obtain the best genes." 

Is it, in fact, common for a child's biological father to be someone other than the social father? No reliable studies seem to be available, no doubt in part because of the severe ethical difficulties of trying to conduct one. But when testing family members for inheritable diseases, genetic counselors stumble across evidence of discrepant paternity surprisingly often. 

For the population as a whole, "The generic number used by us is 10 percent," said Dr. Bradley Popovich, vice president of the American College of Medical Genetics, although he guesses it is less in Oregon, where he directs a genetic diagnostic laboratory at the Oregon Health Science University. 

Discrepant paternity would suggest that some women may exercise a certain selectivity in the choice of a biological father, but it does not prove the condition for sperm competition, which is insemination by two or more men within the few days that sperm are viable. From a questionnaire asking 4,000 women in Britain how often they had sex with two different men within a space of five days, Dr. Baker estimated that 4 percent of British children were born as a result of sperm competition -- far less than in chimpanzee societies, where probably most infants are conceived this way, but probably enough to exert selective pressure on the evolution of sperm. 
 

"A lot of primatologists 10 years ago said everything is run by the males," Dr. Baker noted, but his and other biologists' evidence now point toward a more powerful though less obvious role for women. "They are showing subterfuge and mating with males in secret to their own best advantage," he said. 

Dr. Baker, however, is ahead of most primatologists, who see a clear distinction between human and chimpanzee mating systems. Even though the two species shared a common ancestor only five million years ago, fossil evidence shows that the male-female size ratio in humans has been the same for the last 1.9 million years, Dr. Wrangham said. This suggests the mating system too has remained constant, and different from the chimp's, for the same period. 
 

The film, fashion and fiction industries promote the notion that people are great lovers. Those familiar with Bacchanalian romps of chimpanzees have a less heroic view of human sex lives. "Despite the desire of human beings to believe we are very sexy, we don't have very frequent copulatory behavior compared to macaques, chimps and bonobos," Dr. Dixson said. 

For primatologists, human sperm competition is still unproved, and their milquetoast appraisal of the species' mating system -- "mildly polygynous" -- suggests a not so daring excursion from plain monogamy.