Why is Sex Fun?: the evolution of human sexuality

There is no question that the many-fathers theory is plausible for those animal species (and perhaps those traditional human societies) in which infanticide is a big problem. But the theory seems hard to reconcile with modern human society as we know it. Yes, extramarital sex occurs, but doubts about paternity remain the exception, not the rule that drives society. Genetic tests show that at least 70 percent, perhaps even 95 percent, of American and British babies really are sired legitimately, that is, by the mother's husband. It's hardly the case that for each kid there are many men standing around radiating benevolent interest, or even showering gifts and dispensing protection, while thinking, “I may be that kid's real father!”
It therefore seems unlikely that protecting kids against infanticide is what propels women's constant sexual receptivity today. Nevertheless, as we'll now see, women may have had this motivation in our distant past, and sex may have subsequently assumed a different function that now sustains it.
How, then, are we to evaluate these two competing theories? Like so many other questions about human evolution, this one can't be settled in the way preferred by chemists and molecular biologists, a test-tube experiment. Yes, we'd have a decisive test if there were some human population whose women we could cause to turn bright red at estrus and to remain frigid at other times, and whose men we could cause to be turned on only by bright red women. We could then see whether the result was more philandering and less paternal care (as predicted by the daddy-at-home theory) or less philandering and more infanticide (as predicted by the many-fathers theory). Alas for science, such a test is presently impossible, and it will remain immoral even if genetic engineering ever makes it possible.
But we can still resort to another powerful technique preferred by evolutionary biologists for solving such problems. It's termed the comparative method. We humans, it turns out, aren't unique in our concealment of ovulation. While it's exceptional among mammals in general, it's fairly common among higher primates (monkeys and apes), the group of mammals to which we belong. Dozens of primate species show no externally visible signs of ovulation; many others do show signs, albeit slight ones; and still others advertise it flagrantly. The reproductive biology of each species represents the outcome of an experiment, performed by nature, on the benefits and drawbacks of concealing ovulation. By comparing primate species, we can learn which features are shared by those species with concealed ovulation but are absent from those species with advertised ovulation.
That comparison throws new light on our sexual habits. It was the subject of an important study by the Swedish biologists Birgitta Sillen-Tullberg and Anders Moller. Their analysis proceeded in four steps.
Step 1. For as many higher primate species as possible (sixty-eight in all), Sillen-Tullberg and Moller tabulated visible signs of ovulation. Aha! — you may object immediately-visible to whom? A monkey may give signals invisible to us humans but obvious to another monkey, such as odors (pheromones). For example, cattle breeders trying to perform artificial insemination on a prize dairy cow have big problems figuring out when the cow is ovulat-ing. Bulls, though, can tell easily by the cow's smell and behavior.
Yes, that problem can't be ignored, but it's more serious for cows than for higher primates. Most primates resemble us in being active by day, sleeping at night, and depending heavily on their eyes. A male rhesus monkey whose nose isn't working can still recognize an ovulating female monkey by the slight reddening around her vagina, even though her reddening is not nearly so obvious as in a female baboon. For those monkey species that we humans classify as having no visible signs of ovulation, it's often clear that the male monkeys are equally confused, because they copulate at totally inappropriate times, such as with non-estrous or pregnant females. Hence our own ratings of “visible signs” aren't worthless.
The result of this first step of the analysis was that nearly half of the primates studied-thirty-two out of sixty-eight-resemble humans in lacking visible signs of ovulation. Those thirty-two species include vervets, marmosets, and spider monkeys, as well as one ape, the orangutan. Another eighteen species, including our close relative the gorilla, exhibit slight signs. The remaining eighteen species, including baboons and our close relatives the chimpanzees, advertise ovulation conspicuously.
Step 2. Next, Sillen-Tullberg and Moller categorized the same sixty-eight species according to their mating system. Eleven species-including marmosets, gibbons, and many human societies-turn out to be monogamous. Twenty-three species-including other human societies, plus gorillas-have harems of females controlled by a single adult male. But the largest number of primate species-thirty-four, including vervets, bonobos, and chimpanzees-have a promiscuous system in which females routinely associate and copulate with multiple males.
Again I hear cries of Aha! — Why aren't humans also classified as promiscuous? Because I was careful to specify routinely. Yes, most woman have multiple sex partners in sequence over their lifetimes, and many women are at times involved with multiple men simultaneously. However, within any given estrus cycle the norm is for a woman to be involved with a single man, but the norm for a female vervet or bonobo is to be involved with several partners.
Step 3. As the next-to-last step, Sillen-Tullberg and Moller combined steps 1 and 2 to ask: is there any tendency for more or less conspicuous ovulations to be associated with a particular mating system? Based on a naive reading of our two competing theories, concealed ovulation should be a feature of monogamous species if the daddy-at-home theory is correct, but of promiscuous species if the many-fathers theory holds. In fact, the overwhelming majority of monogamous primate species analyzed-ten out of eleven species-prove to have concealed ovulation. Not a single monogamous primate species has boldly advertised ovulations, which instead are usually (in fourteen out of eighteen cases) confined to promiscuous species. That seems to be strong support for the daddy-at-home theory.
However, the fit between predictions and theory is only a half-fit, because the reverse correlations don't hold up at all. While most monogamous species have concealed ovulation, concealed ovulation in turn is no guarantee of monogamy. Out of thirty-two species with concealed ovulation, twenty-two aren't monogamous but are instead promiscuous or live in harems. Concealed ovulators include monogamous night monkeys, often-monogamous humans, harem-holding langur monkeys, and promiscuous vervets. Thus, whatever caused concealed ovulation to evolve in the first place, it can be maintained thereafter under the most varied mating systems.
Similarly, while most species with boldly advertised ovulations are promiscuous, promiscuity is no guarantee of advertisement. In fact, most promiscuous primates— twenty out of thirty-four species-either have concealed ovulation or only slight signs. Harem-holding species as well have invisible, slightly visible, or conspicuous ovulations, depending on the particular species. These complexities warn us that concealed ovulation will prove to serve different functions, according to the particular mating system with which it coexists.
Step 4. To identify these changes of function, Sillen-Tullberg and M0ller got the bright idea of studying the family tree of living primate species. They thereby hoped to identify the points in primate evolutionary history at which there had been evolutionary changes in ovulatory signals and mating systems. The underlying rationale is that some modern species that are very closely related to each other, hence presumably derived recently from a common ancestor, turn out to differ in mating system or in strength of ovulatory signals. This implies recent evolutionary changes in mating systems or signals.