The Myth of Monogamy: Fidelity and Infidelity in Animals and People (22 page)

Female EPCs can also be constrained by direct costs borne by the females. In Chapter 2, we considered possible costs to EPC-seeking males: being cuckolded by other males while you are away from home, being injured by your lover's mate, simply wasting time and energy if you are unsuccessful or if your lover isn't fertile. There is reason to think that the downsides of EPCs are more pronounced for females.

One possibility is sexually transmitted disease. The risk is notorious, especially for human beings in the age of AIDS. (Although, clearly, venereal diseases preceded AIDS, with gonnorhea and syphilis--and, more recently, herpes--being ancient scourges of those whose sexual adventuring transcended monogamy.) It seems likely that EPCs among animals, too, pose potential health risks, although it is remarkable how little we know about venereal diseases among free-living animals.

Males are generally rather bold when out cruising for possible extra-pair copulations, whereas, in nearly all species, females are furtive, often downright secretive. "Open marriages" are exceedingly rare in the natural world; when females engage in an EPC, it is pretty much only when their partners are absent. Indeed, such secretiveness also explains why EPCs were generally not observed by biologists studying the behavior of free-living animals, even after literally thousands of observation hours. If females are attempting to deceive their mates, they are likely to be even more successful with human observers, who are probably far more obtuse! (To this must be added an important point about the intersection of science and psychology: Even in so strictly a "reality-driven" enterprise as natural science, most of us tend to wear intellectual blinders, often failing to recognize something until we first have an explanation for it... or at least, an expectation of it. Believing is seeing.)

The fact that EPCs are nearly always hidden strongly suggests that male detection of such behavior is costly for the females. For example, in a study of red-winged blackbirds in the state of Washington, Elizabeth Gray found that fully 78 percent of all EPCs occurred when the female was away from the territory where she was nesting. EPCs took place either on the territory of the extra-pair male or off the marsh altogether. That is, in this species, extra-pair trysts are most likely to occur either at "his place" or at some neutral site. (Are there red-winged blackbird equivalents to cheap motels?)

Since animal copulations often require only a few seconds, they are sometimes surreptitiously and seamlessly squeezed into the crevices of an otherwise normal day. In contrast to male-female social units, which are normally formed only after the extensive give-and-take of lengthy and

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conspicuous courtship, EPCs are the animal equivalent of what author Erica Jong memorably dubbed a "zipless fuck," a sexual exchange so quick and transitory that the participants hardly even bother to unzip their clothes.

British behavioral ecologist Nick Davies tells the following anecdote: A pair of dunnocks had been feeding together, hopping peacefully toward a bush. Reaching it, the male proceeded to one side, the female to the other. Once out of the male's field of vision, the female instantly flew into the nearby undergrowth, where she copulated with a different male dunnock who had been hidden there. Immediately afterward, the female flew back to the bush, emerged arourid the side, and rejoined her mate, all the while acting as though nothing had happened.

Similar patterns are often observed among nonhuman primates, especially various species of macaque monkeys: The female copulates rather hurriedly behind a rock, tree, or bush, while her consort is temporarily distracted or otherwise unaware of what is transpiring. Immediately afterward, the extra-pair male will often cover his still-erect penis with a hand, as though to hide the evidence from the cuckolded male. All the while, Mrs. Macaque assumes a pose of almost comical nonchalance.

Why all the secrecy?

One possibility is that the outraged male will attack the female, punishing her physically for her infidelity. Surprisingly, perhaps, this has very rarely been documented. One exception is David's research on the "Male Response to Apparent Female Adultery in the Mountain Bluebird." In this study, he attached a model of a male mountain bluebird near two different nests occupied by mated pairs; while the male was away foraging. Upon returning, each male was confronted with the appearance that his female had been sexually unfaithful. In each case his response was to attack the model quite vigorously; not only that, but in one instance the male bluebird actually attacked his mate as well, pulling out two primary flight feathers. She left and was replaced by another female, with whom the male subsequently reared a brood. (The researcher, duly chastened, and not wanting to continue in the role of Shakespeare's Iago, did not interfere additionally in the connubial bliss of this particular Othello. His Desdemona was presumably still alive, although residing elsewhere.)

In this case, the male attacked his mate immediately after attacking the model of an intruding male; his chastisement of his seemingly unfaithful-- but actually innocent--mate.may have been due to unappeased aggression, which was aroused by the model but not fully discharged, since the model did not fight back. In the case of real-life EPCs, the outraged "husband" may be more likely to vent his fury on the other trespassing male than on the "errant wife." Also, each species presents a slightly different situation. Mountain bluebirds nest in empty holes in trees; because such nest-sites are rare, there is typically a reservoir of unmated female mountain bluebirds

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available to mate with a male who has driven out a suspected adulteress. Among most other species, males may not have the luxury of responding so aggressively. Their most effective countermeasure appears to be a withdrawal of parental assistance. It is not a trivial threat.

Being a single parent is difficult, whether among animals or human beings. Indeed, the advantage of two parents over one seems to be the main reason why social monogamy occurs at all. Given that, in most species, females make the bulk of the parental investment, they are especially vulnerable to being left holding the bag--for our purposes, holding the babies--without assistance from their mate. In other words, among birds and mammals there is a much greater risk that females will be abandoned by their mates and left to be single mothers than that males will be stuck with being single fathers. And among the risk factors that seem likely to contribute to abandonment, EPCs rank very high. After all, males are unlikely to invest time and energy, or to undergo substantial risk, in caring for someone else's kids.

In Rodgers and Hammerstein's classic Broadway musical
Oklahoma!,
there is a marvelous duet sung by the two comic leads, Ado Annie (the "Girl Who Cain't Say No") and her betrothed, Will Parker. Will chastises Annie for her wild ways, demanding that, for them to marry, she must agree to be a chaste, submissive, dutiful wife: "If you cain't give me all, give me nothin', and nothin's what you'll git from me." Annie responds:

I ain't gonna fuss, ain't gonna frown, Have your fun, go out on the town, Stay out late and don't come home till three. And go right off to sleep if you're sleepy ... No use waitin' up for me!

Rather than exceptions, the Ado Annies of the world are abundant, and maybe even the rule. (Hence, this book). At the same time, it is noteworthy that later in the same song, when Annie asks, "Supposing that we should have a third one?" Will responds immediately: "He'd better look a lot like me!"

Female barn swallows who "cain't"--or, at least, don't--say "no," get less help from their mates: WTien females copulate repeatedly with other males, their own mates provide less assistance in rearing their young than when females rarely if ever copulate outside the mateship. Wlien males reduce paternal care in response to female EPCs, females often increase their own maternal care, but frequently not enough to compensate entirely; as a

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result, their offspring are often short-changed. In other cases, compensation by the female is apparently complete, although females seem likely to suffer in the long run, probably through reduced survival rates during the non-breeding season or a diminished life span.

Although eastern bluebirds are normally monogamous--at least socially--when males were experimentally removed, the remaining single-parent females were as successful at rearing offspring as were dual-parent bluebird families. This ability and inclination on the part of female bluebirds to make up for male absence may have the paradoxical effect of encouraging males to wander in search of EPCs. It also suggests that even in some socially monogamous species, females might not be as utterly dependent on males as previous researchers had assumed... although, once again, it remains possible--even likely--that when females are forced to make up for their mate's absence, they ultimately suffer in the long run, perhaps by having a shorter life span.

The risk that males may reduce their parental contribution may limit the degree to which females pursue EPCs, especially in species with biparental care. Fulmars and kittiwakes are colonial-breeding seabirds for whom cooperation between males and females is essential in order for nestlings to be reared. Among these species, EPCs are notably rare, perhaps because the cost of detection is too high to be worth the risk.

On the other hand, the well-studied red-winged blackbirds are typically polygynous, but not necessarily monandrous. Since most females are mated to males who have other "wives," they are already adapted to caring for their young single-handedly. And not surprisingly, EPCs are comparatively frequent in this species, since females have less to lose. This is not to say that the male's contribution is trivial, however. In a population of red-winged blackbirds studied in eastern Ontario, nest defense is the major contribution made by fathers. (Blackbird chicks make a tasty meal for a variety of predators, including crows, gulls, hawks, weasels, raccoons, and mink). Previous research has shown that male swallows are less inclined to defend their young from a stuffed model predator (presented by the experimenter) when their females had earlier engaged in EPCs.

A five-year study of red-wings in eastern Ontario found that the greater the proportion of nestlings sired via EPCs, the less vigorous is the nest defense provided by resident males. Nests in which the putative father had fathered all the young had the highest success rate (number of fledging young). Those in which all the young were sired via EPCs had the lowest. Mixed broods were intermediate. Not only are resident males zealous in defending juveniles in proportion as they have fathered some of them, there is even some evidence that males who sire young via EPCs in other territories are more likely to defend those young.

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These results have not been found in all cases. Indeed, even other populations of the same species, red-winged blackbirds, fall out differently. A study conducted by University of Kentucky biologist David Westneat, for example, found no difference in fledging success between nests with and without extra-pair young. In fact, Westneat found that broods sired by multiple males were
more
successful. Having found no difference in the feeding of nestlings in the two cases, Westneat concluded that mixed-paternity nests did better because the additional males provided, on balance, more paternal defense, not less.

These studies are not necessarily contradictory, however: Let's assume that out-of-pair male red-wings are more likely to help defend their potential offspring if they have had an EPC with the mother. Then it simply becomes a matter of whether the assistance that is forgone (from the resident male, whose confidence in parentage is diminished if he knows of his mate's EPC) is compensated by the additional defense that is obtained (from the extra-pair male).

In most cases, however, it appears that when a female engages in one or more EPCs, she runs a risk that her offspring will receive less paternal care as a result. The salient finding of one research effort was conveyed in the title of the article: "Paternal Investment Inversely Related to Degree of Extra-Pair Paternity in the Reed Bunting." In some cases, males evidently refuse to pay child support if their mate has copulated with someone else. After an EPC that took place in the middle of the female's fertile period, a male magpie abandoned the clutch that he and his mate had been incubating; shortly afterward, he initiated another breeding attempt... interestingly, with the same female. (A second marriage, it has been said, represents the triumph of human hope over experience; maybe something similar can be said of renesting, at least among magpies.)

Young male purple martins, which are often cuckolded by older males, are rather lethargic about feeding "their" nestlings, being significantly less attentive than the females. On the other hand, older male purple martins, cuckolded only rarely, are comparable to females when it comes to fulfilling their parental duties. (It is also possible, of course, that young males just aren't "into" feeding nestlings, whether they have been cuckolded or not.)

Behavioral ecologist Bert Kempenaers relates this story: After a male blue tit was injured--apparently by a sparrow hawk--his mate visited males in several nearby territories and was seen to copulate with at least one of them. She then laid a number of eggs, and a few days later, her mate (the injured male) died. Of the six nestlings produced, DNA analysis revealed that one had been fathered by the deceased male, three had been fathered by the extra-pair male seen to have copulated with the female, and the remaining two had been fathered by another male. Neither of the extra-pair males