For humans, the results of those marriages with advertised ovulations would be awful. Fathers would rarely be at home, mothers would be unable to rear kids unassisted, and babies would die in droves. That would be bad for both mothers and fathers, because neither would succeed in propagating their genes.
Now let’s picture the reverse scenario, in which a husband has no clue to his wife’s fertile days. He then has to stay at home and make love with her on as many days of the month as possible if he wants to have much chance of fertilizing her. Another motive for him to stay at home is to guard her constantly against other men, since she might prove to be fertile on any day that he is away. If the philandering husband has the bad luck to be in bed with another woman on the night when his wife happens to be ovulating, some other man might be in the philanderer’s bed fertilizing his wife, while the philanderer himself is wasting his adulterous sperm on another woman unlikely to be ovulating then anyway. Under this reverse scenario, a man has less reason to wander, since he can’t identify which of his neighbor’s wives are fertile. The heartwarming outcome: fathers hang around and share baby care, with the result that babies survive. That’s good for mothers as well as fathers, both of whom now succeed in transmitting their genes.
In effect, Alexander and Noonan argue that the peculiar physiology of the human female forces husbands to stay at home (at least, more than they would otherwise). The woman gains by recruiting an active coparent. But the man also gains, provided that he cooperates and plays by the rules of his wife’s body. By staying home, he acquires confidence that the child whom he is helping to rear really does carry his genes. He needn’t be fearful that, while he is off hunting, his wife (like a female baboon) may start flashing a bright red derrière as an advertisement for her imminent ovulation, thereby attracting swarms of suitors and publicly mating with every man around. Men accept these ground rules to such a degree that they continue to have sex with their wives during pregnancy and after menopause, when even men know that fertilization is impossible. Thus, in Alexander and Noonan’s view, women’s concealed ovulations and constant receptivity evolved in order to promote monogamy, paternal care, and fathers’ confidence in their paternity.
Competing with this view is the many-fathers theory developed by the anthropologist Sarah Hrdy of the University of California at Davis. Anthropologists have long recognized that infanticide used to be common in many traditional human societies, although modern states now have laws against it. Until recent field studies by Hrdy and others, though, zoologists had no appreciation for how often infanticide occurs among animals as well. The species in which it has been documented now include our closest animal relatives, chimpanzees and gorillas, in addition to a wide range of other species from lions to African hunting dogs. Infanticide is especially likely to be committed by adult males against infants of females with whom they have never copulated—for example, when intruding males try to supplant resident males and acquire their harem of females. The usurper thus “knows” that the infants killed are not his own.
Naturally, infanticide horrifies us and makes us ask why animals (and formerly humans) do it so often. On reflection, one can see that the murderer gains a grisly genetic advantage. A female is unlikely to ovulate as long as she is nursing an infant. But a murderous intruder is genetically unrelated to the infants of a troop that he has just taken over. By killing such an infant, he terminates its mother’s lactation and stimulates her to resume estrus cycles. In many or most cases of animal infanticide and takeovers, the murderer proceeds to fertilize the bereaved mother, who bears an infant carrying the murderer’s own genes.
As a major cause of infant death, infanticide is a serious evolutionary problem for animal mothers, who thereby lose their genetic investment in murdered offspring. For instance, a typical female gorilla over the course of her lifetime loses at least one of her offspring to infanticidal intruding male gorillas attempting to take over the harem to which she belongs. Indeed, over one-third of all infant gorilla deaths are due to infanticide. If a female has only a brief, conspicuously advertised estrus, a dominant male can easily monopolize her during that time. All other males consequently “know” that the resulting infant was sired by their rival, and they have no compunctions about killing the infant.
Suppose, though, that the female has concealed ovulations and constant sexual receptivity. She can exploit those advantages to copulate with many males—even if she has to do it sneakily, when her consort isn’t looking. While no male can then be confident of his paternity, many males recognize that they might have sired the mother’s eventual infant. If such a male later succeeds in driving out the mother’s consort and taking her over, he avoids killing her infant because it could be his own. He might even help the infant with protection and other forms of paternal care. The mother’s concealed ovulation will also serve to decrease fighting between adult males within her troop because any single copulation is unlikely to result in conception and hence is no longer worth fighting over.
As an example of how widely females may thus use concealed ovulation to confuse paternity, consider the African monkeys called vervets, familiar to anyone who has visited an East African game park. Vervets live in troops consisting of up to seven adult males and ten adult females. Since female vervets give no anatomical or behavioral signs of ovulation, the biologist Sandy Andelman sought out an acacia tree with a troop of vervets, stood under the tree, held up a funnel and bottle, collected urine when a female relieved herself, and analyzed the urine for hormonal signs of ovulation. Andelman also kept track of copulations. It turned out that females started to copulate long before they ovulated, continued long after they ovulated, and did not reach their peak sexual receptivity until the first half of pregnancy.
At that time the female’s belly was not yet visibly bulging, and the deceived males had no idea that they were utterly wasting their efforts. Females finally ceased copulating during the latter half of pregnancy, when the males could no longer be deceived. That still left most males in the troop ample time to have sex with most of the troop’s females. One-third of the males were able to copulate with every single female. Thus, through concealed ovulation female vervets ensured the benevolent neutrality of almost all of the potentially murderous males in their immediate neighborhood.
In short, Hrdy considers concealed ovulation an evolutionary adaptation by females to minimize the big threat to their offsprings’ survival posed by adult males. Whereas Alexander and Noonan view concealed ovulation as clarifying paternity and reinforcing monogamy, Hrdy sees it as confusing paternity and effectively undoing monogamy.
At this point, you may be starting to wonder about a potential complication in both the daddy-at-home theory and the many-fathers theory. Why is human ovulation concealed from women as well, when all that’s required by either theory is for women to conceal ovulation from men? For example, why couldn’t women keep their derrières the same shade of red every day of the month to deceive men, while still remaining aware of sensations of ovulation and just faking an interest in sex with lusty men on non-ovulatory days?
The answer to that objection should be obvious: it would be hard for a woman convincingly to fake sexual receptivity if she felt turned off and knew that she was currently infertile. That point applies with particular force to the daddy-at-home theory. When a woman is involved in a long-lasting monogamous relationship in which the partners come to know each other intimately, it would be hard for her to deceive her husband unless she herself were deceived as well.
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.
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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 Sillén-Tullberg and Anders Møller. Their analysis proceeded in four steps.
Step 1. For as many higher primate species as possible (sixty-eight in all), Sillén-Tullberg and Møller 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 ovulating. 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, Sillén-Tullberg and Møller 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, Sillén-Tullberg and Møller 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, Sillén-Tullberg and Møller 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.
Here’s an example of how the reasoning works. We know that humans, chimps, and gorillas are genetically about 98 percent identical and stem from an ancestor (“the Missing Link”) that lived as recently as nine million years ago. Yet those three modern descendants of the Missing Link now exhibit all three types of ovulatory signal: concealed ovulation in humans, slight signals in gorillas, bold advertisement in chimps. Hence only one of those descendants can be like the Missing Link in ovulatory signals, and the other two descendants must have evolved different signals.
In fact, most living species of primitive primates have slight signs of ovulation. Hence the Missing Link may have preserved that condition, and gorillas may have inherited it in turn from the Missing Link (see figure 4.1). Within the last nine million years, though, humans must have evolved concealed ovulation, a
nd chimps must have evolved bold advertisement. Our signals and those of chimps thus diverged in opposite directions from the cues of our mildly signaling ancestors. To us humans, the swollen derrières of ovulating chimps look like those of baboons. However, the ancestors of chimps and baboons must have evolved their eye-catching derrières quite independently, since the ancestors of baboons and of the Missing Link parted company around thirty million years ago.
Family Tree of Ovulatory Signs
Figure 4.1
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By similar reasoning, one can infer other points in the primate family tree at which ovulatory signals must have changed. It turns out that switches of signals have evolved at least twenty times. There have been at least three independent origins of bold advertisement (including the example in chimps); at least eight independent origins of concealed ovulation (including its origins in us, in orangutans, and in at least six separate groups of monkeys); and several reappearances of slight signs of ovulation, from either concealed ovulation (as in some howler monkeys) or from bold advertisement (as in many macaques).
In the same way as we’ve just seen for ovulatory signals, one can also identify points in the primate family tree at which mating systems must have changed. The original system for the common ancestor of all monkeys and apes was probably promiscuous mating. But if we now look at humans and our closest relatives, the chimps and gorillas, we find all three types of mating system represented: harems in gorillas, promiscuity in chimps, and either monogamy or harems in humans (see figure 4.2). Thus, among the three descendants of the Missing Link of nine million years ago, at least two must have changed their mating system. Other evidence suggests that the Missing Link lived in harems, so that gorillas and some human societies may just have retained that mating system. But chimps must have reinvented promiscuity, while many human societies invented monogamy. Again, we see that humans and chimps have evolved oppositely, in mating systems as in ovulatory signals.