The Myth of Monogamy: Fidelity and Infidelity in Animals and People (12 page)

Just as there are sometimes,disputes about whether sex was consensual or forced among human beings, there are gray areas in certain animal cases, too. Males are sometimes aggressive in seeking EPCs, verging on rape, as in the case of indigo buntings. In others--such as black-capped chickadees and blue tits--females actively solicit copulations, while in yet others, males are unquestionably not only initiators, but brutal assailants.

In any event, unattractive and otherwise unsuccessful males are in an especially difficult situation. We have noted that compared to females, the parental investment of males is relatively skimpy, so they are expected to compete with other males and/or to be attractive to females. But what if they are uncompetitive and unattractive? Even if they succeed in pairing with a female, as we shall see in the next chapter, their mates will often take the

54 the myth of monogamy

opportunity of improving their reproductive situation by mating on the sly with more desirable males, whereas these unappealing males may have no comparable recourse, except for rape, since they are likely to be rejected by females if they attempt EPCs, for the same reason that they are liable to be cuckolded by their own mates. There is in fact a growing body of evidence that human rape, too, tends to be a reproductive tactic of likely "losers."

We have already seen that when rape occurs among mallards, paired males often attempt to defend their mates, and when unsuccessful, they frequently respond by raping the victim themselves. This has subsequently been found for many other species as well. WTiy such an ungentlemanly response? Probably because, given "last male advantage" as well as the possible payoff of simply diluting any sperm introduced by the rapists, the mated male is attempting (albeit unconsciously) to increase the chance that he will father any chicks produced.

It is probably no coincidence that mountain bluebird males attacked their mates after they had been deceived as to their fidelity; among this species, there is typically a reservoir of available, unmated females. By contrast, mallard drakes whose females had been raped nearly always remain mated to them; in their case, there is generally a shortage of unmated females, so a drake is better off remaining with a sexually compromised mate than abandoning her and likely ending up with no mate at all.

Actually, the highest recorded frequencies of rape are found in a closely related pair of geese, Ross's goose and the lesser snow goose. Research conducted at the largest known goose colony in the world--consisting of 291,000 Ross's and 297,000 lesser snow geese, on Karrak Lake, Nunavut (formerly part of the Northwest Territories, Canada)--has found that among these attractive, innocent-looking birds, about 50 percent of attempted copulations occur outside the pair-bond, nearly all of them the consequence of rape. About one-third of these rape attempts are successful, in that the attacking male achieves cloacal contact with his victim. But "success" in a biological sense is more elusive: Extra-pair paternity in the two species is consistently less than 5 percent, mostly because rapes occur too late in the breeding cycle, when the victimized females are no longer fertile. Evidently, rape is not an efficient reproductive tactic for male geese, although it pays off in some cases. Even though only 1 attack in 20 produces offspring, it can still be a winning strategy for the rapist if the costs to him are sufficiently low.

Incidentally, not all waterfowl experience high levels of rape. It appears that species that defend a relatively large territory around their nests are less likely to have to deal with sexually motivated intruders. Maybe this is one reason for defending a large territory in the first place. Good fences--

undermining the myth: males 55

or, rather, widely separated territories--may make sexually well-behaved neighbors.

The upshot of all this: Even though monogamy is the primary mating system in mallards, geese, and many of the so-called puddle ducks, the male inclination for additional sexual opportunities has--to coin a phrase--muddied the waters. Just as it has for pretty much all other living things.

Soon, we'll look at our own species. But let's end this chapter by noting that human beings show the entire repertoire of EPC-related male behavior: a penchant for extra-pair copulations, a tendency for mate-guarding, frequent copulation, reduced paternal care in cases of reduced confidence of genetic fatherhood, maybe even anatomic adaptations of the penis and EPC-sensitive adjustments in sperm production. People are also prone to respond to real or suspected adultery by their mates with desertion and even violence. Indeed, adultery--or the suspicion of adultery--is a major cause of divorce, and of spousal violence as well. About one-third of spousal killings in the United States are due to female infidelity, whether correctly attributed or suspected. The frequency of infidelity-generated violence is, if anything, even higher in other societies for which data have been collected, such as Africa.

And yet, in spite of the high risks, female infidelity--along with male philandering--seems to be virtually universal. And not simply as a result of male compulsion.

The usual assumption among evolutionary biologists is that male sexual behavior is geared toward quantity of offspring, whereas its female counterpart is geared toward quality. This, in turn, is achieved by men being oriented toward
quantity
of sexual partners, and women, toward their
quality.
Monogamy, when adhered to, enforces a similar strategy on both men and women. It is in the realm of EPCs, on the other hand, that such male-female differences between quantity and quality are most likely to be revealed.

No one is claiming that males are always or single-mindedly in pursuit of extra-pair sexual opportunities--only that they are predisposed to do so under certain conditions. Furthermore, as we shall see, this seems to apply to
Homo sapiens
no less than to other species. On the other hand, traditional wisdom in evolutionary biology has claimed that females are comparatively coy, choosy, and faithful. They are. But increasingly, we are also learning that females in general--and this includes women in particular-- are not so easily pigeonholed.

The myth of monogamy is seriously threatened, although monogamy as a human institution seems likely to carry on indefinitely, an ancient yet

56 the myth of monogamy

sturdy Potemkin Village behind its long-standing facade of polite fiction. There is little doubt that the majority of males, whether "married" or not, are favorably inclined toward out-of-pair sex. (This does not necessarily mean, however, that they will always act upon it; see Chapter 7.) For a "married" male to engage in out-of-pair heterosexual sex, his EPC partner must in turn be (1) seduced, (2) coerced, (3) a willing co-participant, or (4) an active initiator. And so, we turn to the role of the female. We'll find that all four patterns occur, in animals as well as human beings. ,

CHAPTER THREE

Undermining the Myth: Females (Choosing Male Genes)

Several decades ago, a research team was looking into the prospect of using surgical birth control to reduce populations of unwanted birds. They experimentally vasectomized a number of territorial male blackbirds and were more than a little surprised by the results: A large percentage of the females mated to these sterilized males nonetheless produced offspring! Clearly, there was some hanky-panky going on in the blackbird world: These females must have been copulating with other males, not just with their social mates.

Long before DNA analysis and the formal identification of EPCs, tantalizing findings such as this suggested that the traditional teaching among evolutionary biologists needed some revision. It had long been thought that females of most species were the "flip-side" of males: Their yearning for cozy monogamous domesticity was supposed to be about as strong as the male tendency to mate with as many different partners as possible. Whereas males were known to gallivant and try to sow their wild oats, their "wives," it was assumed, stayed home--at the nest or den--minding the hearth, dutifully bearing young fertilized by their "husbands." The males had a fondness for philandering; females supposedly did not.

This expectation of a double standard in the animal world may have been soothing to the ego and also perhaps to the unspoken anxieties of many biologists ... the majority of whom have long been male. But DNA fingerprinting and associated technologies have changed all that forever,

58
the myth of monogamy

confirming that, at least in some cases, females practice less than perfect sexual fidelity.

In
The Descent of Man and Selection in Relation to Sex
(1871), Charles Darwin wrote that "the males are almost always the wooers" and that "the female, though comparatively passive, generally exerts some choice and accepts one male in preference to the others." As we now understand it, Darwin was correct... as usual. But he must be taken more literally than one might think. Thus, it is not true that females accept one male and only one male, period. Rather, as Darwin pointed out, females accept one male in preference to the others ... while often trying out the others, too! Female "preference," in this context, may mean giving an edge to the genetic contribution of one male rather than another, but this assuredly does not require monastic sexual fidelity on the part of the female. Coyness may have its value as public policy--the stance most females assume in front of strangers and, notably, their acknowledged social and sexual partner--but it does not necessarily reflect what they do in private.

Of course, the mere fact of extra-pair copulations does not in itself indicate female
choice:
In some cases, female animals no less than human beings are raped. But in many others, they actively solicit sexual relations with males who are not their acknowledged social partner. Female primates, for example, may temporarily leave their troop or--if ostensibly monogamous--their male "significant other" to hang out with one or more neighboring males; similarly, birds may fly onto the territories of other, already mated males, typically early in the morning. In such cases--and especially when genetic testing subsequently reveals that one or more of her offspring have been fathered by a male other than her presumed mate--there can be no mistaking either her behavior or her motivation ... not unlike a woman who "just happens" to visit a man's hotel room late at night.

It remains true that the sexual tactics of males differ from those of females, being more showy, pushy, outwardly competitive, and sometimes even violent. In addition, just as not all males are philanderers, there are some cases in which females vigorously rebuff the extracurricular mating efforts of other males, suggesting that EPCs are not always in a female's interest. Nonetheless, the evidence has been accumulating, fast and furious, that females are not nearly as reliably monogamous as had been thought-- and that often they are active sexual adventurers in their own right.

Why?

One possibility is that extra-pair copulations by females are nonadap-tive, an unavoidable by-product of strong selection for multiple mating by males. Thus, perhaps any female penchant for EPCs is merely the equivalent of nipples in male mammals, a tag-along trait that has no value in itself but

UNDERMINING THE MYTH: FEMALES (CHOOSING MALE GENES)
59

is maintained simply because it is advantageous in the opposite sex and somehow cannot avoid being expressed in both sexes, even though it is only meaningful in one.

An interesting idea, this, but one that is not supported by the evidence, especially since male and female mating tendencies are not genetically correlated; in other words, selection for high mating frequency in one sex does not necessarily produce high mating frequency in the other.

We are stuck with the question:
Why
aren't females more monogamous?

It is relatively easy to understand the evolutionary payoff that males derive from playing fast and loose. All other things being equal, more copulations mean more opportunities for them to project their genes into the future, and--usually--at relatively little cost. But what do females get out of EPCs? A tempting answer is simply that "they like it," or maybe "they find it exciting" or "interesting," or perhaps "it feels good." In evolutionary terms, however, these are all inadequate explanations, just as it is insufficient to explain sleep, for example, by saying that it is a response to being tired.

For sleep researchers, a crucial question is:
Why
does prolonged wakefulness make people tired? Tiredness is simply an internal state that leads people, under certain circumstances, to seek sleep; it is not an explanation in itself. Tiredness says nothing about the adaptive significance of sleep or about the mechanisms of sleep and, hence, why tiredness is a prelude to it. Similarly, for evolutionary biologists, it is not sufficient to say that females seek extra-pair copulations because they "like" it or because they sometimes find other males attractive. The crucial question is: Why do females of many species that are socially monogamous engage, at least on occasion, in extra-pair copulations? Another way of saying this:
Why
do they "like" it?

The one-size-fits-all adaptive explanation is that EPCs must somehow contribute to the ultimate reproductive success of the females that do it. The challenge, then, is to identify how this increased success comes about.
What
is the payoff to such females?