The Myth of Monogamy: Fidelity and Infidelity in Animals and People (36 page)

In at least one primate species, females clearly use sex as an inducement for males to act paternally. A field study has found that female saddle-backed tamarins (small primates of the New World rain forests), if given the opportunity, will mate with more than one adult male. Mrs. Tamarin will then give birth to twins, and a different male will proceed to assist her in caring for each infant. By spreading the breeding and giving each male an interest in her babies, the tamarin mother-to-be appears to spread the subsequent child-care duties among willing males.

For most females, genetic partners are easy to come by. Behavioral partners are a different story. Males are typically more than willing to contribute some squirts of sperm in return for a chance at reproductive success. Harder to come by are males willing to be behavioral fathers, not just genetic beneficiaries. The optimum female strategy--as in many other species--would be to get the best of each: Mate with genetically promising males and gain other benefits from wealthy, paternally inclined individuals. If all this can obtained from just one individual, so much the better. If not, then a bit of deception may be worthwhile. And concealed ovulation seems to be a useful ticket, offering the opportunity for females to present the appearances of monogamy (and, hence, to get paternal investment from their in-pair mates) while also gaining genetic benefits from out-of-pair copulations.

Of course, concealed ovulation could also be a device permitting women to engage in sperm competition while deceiving each man into thinking that he is the father. Thus, when ovulation is hidden, so is the identity of the father. The payoff, for the mother, is that she can obtain sperm from more than one male, then "choose" which to use to fertilize her egg(s). This has been called "cryptic polyandry," and, as noted, it is all the rage among birds.

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Female blue tits paired to high-quality males--quality measured by anatomical traits such as longer tarsal bones, which correlate with higher survivorship and the likelihood of producing more successful young--remain sexually faithful. And females paired with low-quality males? They are inclined to be socially monogamous, but they also visit the territories of the more desirable males--and mate with them, thereby getting assistance from their in-pair mates but genes from among the best available specimens.

Another thing. Along with concealed ovulation come restraints on estrus. A woman, even at midcycle, is nothing like a bitch in heat. (If she were, then her ovulation wouldn't be concealed!) Concealed ovulation thus offers a new perspective on "reproductive choice," referring not only to a woman's choosing whether, when, or how to terminate her pregnancy, but also whether, when, and with whom to initiate it.

According to primatologist Sarah Hrdy, a female langur monkey "exhibits no visible sign when she is in estrus other than to present to a male and to shudder her head." When she encounters strange males, a female langur has the capacity to shift from cyclical receptivity (that is, a spontaneous bout of heat every 28 days) to a state of semicontinuous receptivity that can last for weeks. This gives females the opportunity to achieve sexual relationships with males other than the harem-keeper, at their own choosing, rather than being captive of automatic estrous cycles--for example, if a new and enticing male joins the troop, if a female happens to leave her troop to travel temporarily with an all-male band, or if, in Hrdy's words, "a female for reasons unknown to any one, simply takes a shine to the resident male of a neighboring troop." Other primates have a similar capacity, including several different species of guenons, vervets, and gelada baboons.

Why
should women be any less endowed and, thereby, empowered? With their ovulation concealed and their sexual motivation under substantial cognitive control, women can select their reproductive partners far more easily than if they were victims of their raging hormones ... as is the case, by contrast, for men!

Orgasm is another story, as complex and unresolved as concealed ovulation. Some, including anthropologist Donald Symons, have suggested that the female orgasm is biologically meaningless, an irrelevant but unavoidable side effect of the (clearly adaptive) male orgasm. If so, it would be analogous to nipples in male mammals--a tag-along trait, as discussed at the beginning of Chapter 3. Others, like the writer Desmond Morris, have proposed that orgasm makes fertilization more likely by encouraging a woman to remain horizontal, thereby making it easier for

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sperm to swim to their goal. The actual effect of female orgasm on fertilization is complex. Certainly, a woman's climax is not needed for conception to occur. Moreover, orgasm actually increases the volume of flowback, in part because it results in increased quantities of cervical mucus. There is also evidence, paradoxically, that too many sperm
reduce
the probability of conception, perhaps because of multiple fertilizations--which are spontaneously aborted--or because of the deleterious effect of chemicals secreted by exceptionally large numbers of sperm milling about.

Some female orgasms appear to increase the amount of sperm retention, whereas others are more likely to extrude sperm. Sexual intercourse itself, on the other hand, has a positive effect on conception, independent of the actual deposition of sperm. Thus, artificial insemination via a sperm donor is more likely to be successful if women alsp engage in sexual intercourse with their partner, even if he is totally sterile. The reason for this effect is unknown, but it emphasizes that the female sexual experience is somehow connected to the probability of conception, although the connection apparently is not a simple one.

For a time, it was thought that the capacity for female orgasm made human beings unique among animals. Not any more. For example, a study of 240 copulations involving 68 different heterosexual pairs of Japanese macaques noted that the females showed all the physiological and anatomical signs of orgasm in 80 cases (exactly one time in three). Neither the age of the female nor her dominance rank correlated with orgasm. On the other hand, the likelihood of orgasm was positively associated with duration of matings and with how active they were (literally, the number of pelvic thrusts by the male). When, by a bit of statistical sleight-of-hand, the researchers analyzed their results, taking these various measures of physical stimulation into account, what emerged was that female orgasm was most frequent among monkey pairs consisting of high-ranking males and low-ranking females, and least frequent among pairs of low-ranking males and high-ranking females. In short, social considerations are important.

This suggests another possible avenue. WTiat if orgasm is a way in which a female's body rewards itself for having done something that is in its own biological interest? Not just mating, but mating with an especially good partner. The idea is that female orgasm, physiologically unnecessary for conception, is useful as an internal signal by which a woman's body rewards her brain for a job well done. Something similar may apply to male orgasm, too. After all, it is not strictly necessary for the pleasurable sensation of ejaculation to exceed that of, say, urinating ... and yet it clearly does. Perhaps the intensity of orgasm says, in effect, "This is not merely a good thing to do, it is a
very
good thing!"

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For men, and males generally, sexual intercourse is a biological plus (especially before the era of AIDS). Hence, a reliable, general-purpose reinforcing mechanism such as orgasm seems appropriate. For women, however, and females generally, sex is easily obtainable, but good sex-- that is, sex with the right male--is harder to come by. Hence, maybe female orgasm is a way for women to confirm that their current sexual partner is especially suitable. Not necessarily as a long-term mate, mind you, just as a mate. Perhaps an ongoing EPC partner. By a process foreshadowed by the "sexy son hypothesis" among animals, maybe female orgasm is how a woman's body italicizes that her current sexual partner-- demonstrated to be capable of providing substantial sexual satisfaction-- might well produce offspring capable of being similarly gratifying to other women, and thus likely to be associated with her long-term reproductive success. (It may also be significant that female orgasm is seen as gratifying to the man as well, and perhaps not just as a confirmation of his own sexual technique.)

It is worth noting that dominant male animals are typically less rushed and more deliberate about sexual intercourse, whereas social subordinates tend to be harried and thus hurried. Thus, we have watched dominant male grizzly bears copulate with sows in a manner that, if not altogether relaxed, at least indicates a degree of control, sexual no less than social. By contrast, subordinate male grizzlies spend much of their copulation time literally swiveling their heads over their shoulders, worrying about the imminent approach of dominant boars! There is no evidence that grizzly sows experience orgasm, but if they did, which type of boar would seem most likely to evoke such a response?

Sexual jealousy is a give-away. Its widespread existence suggests strongly that EPCs--that is, episodes of infidelity--have long been an important part of the human evolutionary past. There would be little reason for such a deep-seated tendency if it were not, to some extent, justified by events.

When a male bighorn sheep is alone with an estrous female, his courtship is likely to be comparatively slow and gentle; when rival males are present, the same male is likely to be more aggressive and brusque. Male rhesus monkeys will routinely attack females caught mating--or just consorting--with lower-ranking male rivals. Sometimes the females are severely injured. In one case, a female rhesus monkey who repeatedly approached another male was fatally injured by her top-ranking male consort. A male hamadryas baboon uses coercion to keep his small harem of females away

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from other males. If one of them happens to stray in the direction of other males, he threatens her with a conspicuous "eyebrow flash." If the errant female doesn't immediately mend her ways and approach the male, he will attack her with a vigorous neck-bite. There have been many other reports-- especially for primates--of males herding their mates away from strange males, particularly during encounters with other groups.

A study of crab-eating macaques in captivity found that male aggression toward females occurred at the relatively low rate of once every three or four hours, so long as the individuals were housed in isolated pairs. When a rival male was introduced, the frequency increased to more than seven times per hour! There is a subtle difference of interpretation involved here. In the past, we assumed that male aggression toward females was simply intended to keep them away from horny and intrusive males. (The focus was on the behavior of
males,
whether seeking EPCs or concerned with mate-guarding.) Now, biologists have begun to see that such aggression is designed to prevent
females
from involving themselves with these other males. (The focus is increasingly on the behavior of
females
seeking EPCs.)

It is prominent among chimps as well: Jane Goodall reports that males are especially likely to "punish" a female who has been sexually involved with another male. Moreover, male chimpanzees sometimes use violence to force a female to follow them; they may spend considerable time herding a female away from other males, displaying substantial aggression toward her during that time. One male--Evered by name--spent five hours directing a female (Winkle) on a forced march, during which time he threatened her numerous times and physically attacked her five times, injuring her on two occasions. As the male increasingly gets his way, and the female is moved far from other males, he relaxes perceptibly. At the same time, the female-- being more dependent on her persecutor/protector--typically becomes more cooperative and pliable. (The obvious human parallels are worrisome but, for all that, no less likely to be genuine.)

Regrettably--at least, by human standards--male chimps who are not sexually pushy and aggressive are generally less successful in consorting with females. In Goodall's account, an adult male named Jomeo was a perfect gentleman, showing the lowest rate of "punitive aggression" toward females. He was also the least successful when it came to forming consortships, and he appears to have been the only adult male who did not sire any offspring. Goodall speculates that males are often aggressive toward females in order to facilitate later sexual relationships: To the extent that a female is readily intimidated by given male, that male is more likely to obtain her sexual acquiescence in the future. Not a pretty picture, but one that comes more clearly into focus when we consider the role of

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EPCs in predisposing males, in this case, to use aggression and even violence to force themselves upon females who might well have someone else in mind.

In short, it may be that some of the ugliest human behavior--marital abuse, wife beating, even homicide--derives at least in part from a widespread biological propensity to depart from monogamy.

Time now to summarize. (Easier said than done!) Human beings are unusual in their mating system. Although for the most part
Homo sapiens
is socially monbgamous, displaying--for a mammal--huge amounts of paternal care, people also live almost colonially, often in enormous groups. In our social monogamy, we are like gibbons, yet we are also like chimps in that women interact regularly with other adults, not only other women but even other men. Sex, in such cases, may well be in the background, and for the most part that is where it stays. In some ways, we are more like certain colonial birds: socially monogamous yet rubbing shoulders with lots of other adults, every day. In such species, when males and females spend long periods of time apart from each other--one foraging, for example, while the other is attending the nest--both males and females have abundant opportunities for EPCs.