The Myth of Monogamy: Fidelity and Infidelity in Animals and People (15 page)

In one type of beetle, the female remates more readily with a new male than with her previous partner, which suggests that she, too, is looking for genetic benefits associated, in all likelihood, with enhanced variety. In some insects, the female deposits an identifying odor on the male, allowing her to discriminate against him when it comes to remating!

Most commonly, however, it appears that females choose males with "good genes," as shown by the fact that males with larger sexual ornaments produce more viable offspring (e.g., peacocks). But how to reconcile this with multiple mating by females? If females are choosing the best male, why mate with more than one? Recall that a female may simply not be able to settle down and raise a family with the male of her dreams; he may already be taken. In this case, EPCs provide the opportunity for females to bond with one male--and indeed to rear children with him--but to copulate with another, and thereby obtain his genes.

70
the myth of monogamy

Another possibility is to mate with your social partner, but do so again-- and yet again, perhaps--with a more preferred male, if he shows up. Such "ratcheting" is not female promiscuity, by the way, because these females are not being sexually indiscriminate. Far from it. They are carefully evaluating the merits of their potential sexual partners, seeking to trade up when possible. Other cases, like that of the pseudoscorpions, where females cannot evaluate the quality of males and simply go for novelty, are closer to promiscuity. But even here, there is method to their sexual meandering. Virgin pseudoscorpions, for example, invariably pick up the first sperm packet deposited by a male; after this, 88 percent reject his
next
sperm offering. It isn't that such females have suddenly become uninterested in mating, however: Exposed to a new male shortly afterward, they again pick up his first sperm packet... and then refuse his subsequent ones. They're just uninterested in mating with the same male twice!

The most frequent pattern reveals not so much a preference for diversity as a predilection for quality. Male house sparrows, for example, possess dark throat badges, indicators of their macho qualities--and female house sparrows are more likely to have EPCs with males sporting large throat badges than with those whose throat badges are less impressive.

Most of the time, moreover, females choose their EPC partners from among the ranks of married males--who are likely to be of higher quality-- rather than mating on the side with bachelors, who are generally bachelors for good reasons (that is, they were unsuccessful in obtaining a mate in the first place because of being lower quality).

Not only that, but females tend to select as EPC partners those males who are in some way superior to their current mates. Among zebra finches, females evaluate the sexual desirability of a male by the brightness of his bill color; they solicit EPCs only from males whose bills are not only bright, but brighter than those of their current mates.

Many female birds get to choose their mates in order as they--the females--arrive on the breeding territories; earlier-arriving females should therefore get the most desirable males, and later-arriving ones should be more likely to seek out EPCs. This appears to be the case.

If genetic diversity were the reason for EPCs, then females of species that produce only one egg per year should attempt EPCs only in some years, not each year. (One offspring with a given male cannot be more diverse than one offspring with another male!) On the other hand, if females are seeking genetic quality, they should be motivated to obtain such quality each year.

undermining the myth: females (choosing male genes)
71

A study of razorbills, an ocean-going bird that produces only one egg per year, found that the females' inclination for EPCs remained consistent year to year. This supports the hypothesis that they are seeking quality rather than diversity.

The prevalence of EPCs is highly variable, from zero in some species to nearly 100 percent in others. Even within any one species, there are typically differences between male and female participation in EPCs, the general pattern being a higher proportion of female than of male involvement. It is not uncommon, for example, for about 15 percent of females, but only 7 percent of males, to engage in EPCs. This harkens back to the earlier generalization by sociobiologists that males are more variable in their reproductive success than are females, since a small proportion of males "enjoy" reproductive success that goes beyond their own pair-bond. Presumably, those that do so are especially desirable to the females in question. The chances are that any female willing to take the risks of an EPC would be able to obtain it, whereas males generally yearn to be called, but only few are chosen.

An important consideration--for both males and females--is the breeding system itself, for example, whether there are other "helpers" available to assist with child care. Fairy-wrens of Australia often breed cooperatively, with all males contributing to the feeding and defense of the young. DNA fingerprinting shows that more than 75 percent of the offspring are actually fathered by males outside the group, who provide no parental care, and that 95 percent of all broods contain young sired by extra-group fathers. This is the highest incidence of animal cuckoldry of which we are aware. Female fairy-wrens are very much in charge of whom they mate with: They successfully avoid all EPC attempts initiated by outside males, only mating when they initiate and solicit. And they are highly selective. Of 68 out-of-group potential fathers identified in one study, just 3 fathered nearly 50 percent of all the extra-pair offspring. As a result of such choice (and, in all likelihood, the reason for it as well), sons produced via EPCs are highly successful in obtaining EPCs.

Fairy-wrens do not always form large breeding groups. In some cases, they mate in pairs; in these situations, the paired male has a much higher chance of being the biological father than does the dominant male in a communally breeding group. Paired males also contribute much more to rearing their offspring, as predicted by the fact that they are likely to be the fathers. In communal breeding groups, females get less help from any given male, but, in return, they gain freedom of reproductive choice, via EPCs. When female fairy-wrens have helper males available--the group situation--they are liberated to choose good genes from outside the group. (Incidentally,

72
the myth of monogamy

these helpers are generally sons of the female; hence they gain an indirect genetic payoff from their mother's breeding success--no matter who the father is--while the adult female likely gains by being sexually liberated to choose the best possible EPC partner.).

Not surprisingly, females of any species that are sitting pretty, mated to an especially well-endowed male, are less inclined to stray sexually, whereas those whose mates are less desirable are more likely to try one or more EPCs .. .and when they do so, to insist on "moving up," reserving their extracurricular mating for those males who offer a better genetic package than their current mate.

et's assume that, at least in some cases, females are in fact choosing good genes. What, precisely, does this mean? How can one set of genes be better than another? In lots of ways.

For one, good genes could simply be those that lead to healthier offspring. Probably the best example of this comes from research conducted by Allison Welch, then a graduate student at the University of Missouri, Columbia, and her colleagues. They studied gray tree frogs, a species in which females prefer to mate with males whose songs are comparatively lengthy (about two seconds long) rather than very brief (about one second long). By acting on this preference, females get good genes, leading to offspring who are more fit. Welch and associates fertilized female eggs with sperm from long- and short-calling frogs, then compared the resulting offspring both as tadpoles and after they had metamorphosed into frogs. The key result: The offspring of long-callers fared better. The key interpretation: Long-calling male gray tree frogs produce offspring that are more likely to survive and, eventually, reproduce. Accordingly, females are well advised to mate with long-callers rather than short callers ... which they do.

Many animals are brightly colored, and often the males are especially adorned. It has been suggested that bright coloration has evolved among males as a cue allowing females to choose as extra-pair partners those males that are especially healthy--parasite-free or parasite-resistant. The saga continues: Among yellowhammers--a species of European finch in which males are bright yellow and females are comparatively drab, and in which old, colorful males are especially successful in obtaining EPCs--the more brightly colored the male, the less likely he is to be infected by parasites. At the same time, the dullest, least-yellow males are most likely to be cuckolded. Among yellowhammers, the brightest, yellowest males are also the oldest, so degree of yellowness and brightness is a reliable indicator that one is carrying genes conducive to longevity.

undermining the myth: females (choosing male genes)
73

Adding to the emerging picture of females engaging in EPCs so as to accrue "good genes" is the fact that species with a high frequency of EPCs are especially likely to be sexually dichromatic (substantial male-female differences in coloration) and to have large spleens for their body size: This suggests a proportionately more well-developed immune system. Such a correlation does not strictly prove anything, but it is consistent with the notion that females in such species seek EPCs in order to obtain greater disease and parasite resistance for their offspring.

An underlying assumption connecting these examples is that males that are especially healthy, and whose health is to some extent heritable, will be preferentially chosen by females as EPC partners. We might define an "attractive" male as one who is visited by many neighboring females, in search of EPCs, and an "unattractive" male as one who is not comparably visited and, thus, who is not in comparable demand. It is then also revealing that females associated with attractive males do not leave their male prospecting for EPCs, whereas females associated with "unattractive" males (that is, those who are not visited by other females) frequently visit their male neighbors.

How, one might ask, do females judge the quality of their mate? And, similarly, how do they judge the quality of their neighbors and possible EPC partners in comparison? A group of Dutch researchers recount one suggestive event: "A male [blue tit] injured one wing just before egg-laying. His female visited both neighbors and both shared paternity with the territorial male. After the young hatched, the territorial male died." All told, of the five males that died between 1 and 3 weeks after their female started incubation, four had a high proportion of extra-pair young in their nest (
⁵
/6,
²
/io,
³
/3,
⁴
h).
It is entirely possible that females use the condition of a male during the breeding season as a clue to indicate his quality and, in turn, use their male's quality as a key determiner of whether or not to seek EPCs.

In at least two other bird species--tree swallows and blue tits--females mated to males that are of comparatively poor quality are more actively involved in seeking EPCs than are females mated to good-quality males. WTiat constitutes "good quality" in such cases is somewhat problematic. But we are beginning to get some hints. Among blue tits, for example, males differ in their probability of surviving the winter, and males that are less likely to make it during the coming winter are more likely to be cuckolded; similarly, males that do the cuckolding are more likely to overwinter successfully. How do female blue tits distinguish the winter-hardy from the winter-wimps? No one knows. (Yet.)

Even when females do not bestow EPCs on physically distinguished males, they may nonetheless be showing a preference for those likely to be

74
the myth of monogamy

of higher quality, perhaps because they are behaviorally distinguished... and, more often than not, genetically distinguished as well. Nothing succeeds, we are told, like success. And indeed, social success--measured by one's position in a dominance hierarchy--succeeds mightily when it comes to securing extra-pair copulations. (Maybe this is what Henry Kissinger meant when he noted that "power is the best aphrodisiac")

There is a widespread tendency for females to prefer dominant males when it comes to bestowing their EPC favors. Dominant male cattle egrets and white ibis--who are successful in male-male fights--are particularly likely to obtain EPCs. Similarly, among black-capped chickadees (a close North American relative of the European blue tit and a common winter participant at bird-feeders), females reserve their EPCs for males whose dominance status is higher than that of their own mates. Over the course of a 14-year study of black-capped chickadees, ornithologist Susan M. Smith observed 13 apparently successful EPCs done by individuals who were color-banded and, thus, whose identities and social ranks were known. In all 13 cases, the female's EPC partner was higher-ranking than her social mate. No females mated to alpha males ever engaged in an EPC. Not only that, but EPCs are mostly solicited by females--individuals who presumably had to settle for less dominant mates and were trying to make up for this deficit. (There's that ratchet again.)

Chickadees, it should be noted, generally mate for life. Smith observed seven cases of divorce; in five of these, a lower-ranked female deserted her mate and established a new social and sexual alliance with a recently widowed alpha male. Social dominance often increases with age; in addition, older males--if only because they have survived so long--are obviously capable of longevity and may well carry genes that promote longer life. Accordingly, older male red-winged blackbirds are more successful in obtaining EPCs. A similar age-related pattern occurs in the European rook (a relative of the North American crow): Older paired males engage in EPCs with younger females. Could this be because younger females were likely to be paired with younger males ... while preferring older ones?

Let us grant that in many different species, females often seek EPCs with males that are especially attractive and dominant (as well as suitably mature). Although this is probably due to a preference on the part of females for males with good genes, the natural world is tricky. Thus, it is possible that dominant and older males are simply more likely to be available for EPCs because they have more sperm to spare or because, as a result of their dominance, they are less likely to be excluded from the territories of other monogamous males. Although females may well seek-- and get--good genes from such liaisons, this is not the same as guaran-

undermining the myth: females (choosing male genes)
75

teeing that they engage in EPCs with high-quality males in order to obtain such genes.

Nonetheless, the evidence is accumulating and is increasingly persuasive.

In songbirds, a male's quality may itself be reflected in his singing. In the previous chapter, we encountered the European great reed warbler, among which females choose EPCs with males who have large song repertoires: As it happens, the survival of young reed warblers is positively correlated with the size of the genetic father's song repertoire. So there is a practical, immediate significance to more songs: better genes. And as one might expect, females of several species give especially intense copulation displays in response to hearing an elaborate song repertoire. (So perhaps there is something to the old tradition of serenading one's lady love.)