The Myth of Monogamy: Fidelity and Infidelity in Animals and People (6 page)

Much of this success--perhaps all of it--is due to a very strong "last male advantage," especially pronounced in many birds: The last male to copulate with a given female before she lays her eggs enjoys disproportionate success in fertilizing those eggs. Regardless of the mechanism, however, the key point for our purposes is that a small amount of breeding effort on the part of males can yield dramatic returns. ("Last male advantage" also has important consequences for the behavior of females, as we'll see in the next chapter.)

undermining the myth: males 25

Many animal breeding systems are such that a small number of successful males are able to monopolize--at least socially--a larger number of females. In such cases, EPCs could, in theory, level the reproductive playing field if otherwise excluded bachelor males gain some "sneak fertilizations" while the legitimate husbands aren't watching. But, instead, EPCs usually
increase
the differences among males. To be sure, it is now a commonplace that some of the offspring previously attributed to a given male (the "husband," if socially monogamous, or the harem-keeper, if polygy-nous) are likely to have been fathered by someone else. But at the same time, success in achieving EPCs is not randomly spread among males; just as certain males are more successful than others in obtaining social mates, certain males are also more successful than others in obtaining extra-pair copulations and, thus, genuine paternity. Nearly always, it is an already successful husband or harem-keeper who also gets the EPCs. For example, among European red deer (called elk in the United States), it has long been known that harem-masters are remarkably successful, whereas excluded bachelors are, comparatively speaking, evolutionary losers. Now, DNA fingerprinting shows that the actual difference between genetic "haves" and "have-nots" is even greater than what had earlier been estimated based on behavioral evidence alone.

Part of the reason for the success of EPC-ing males may lie in this observed fact: Compared with a female's regular sexual partner, they actually produce more sperm at a given copulation, especially if they have not mated recently. In one study involving birds, this was measured by the ingenious if indelicate procedure of persuading males who had been abstemious for different time periods to copulate with a freeze-dried female who had been fitted with a false cloaca.

We don't know whether sperm numbers tend to be generally higher during EPCs than IPCs for mammals as well, nor whether this holds for human beings. We do know, however, that men generally report a higher level of sexual excitement with a new partner (remember the Coolidge effect). Since IPCs, by definition, cannot be with a new partner--except once--it is at least possible that EPCs involve, on average, the production of more sperm per ejaculation among human beings, too. If so, it would make human EPCs more likely to result in offspring than chance alone would predict. Needless to say, this speculation will be difficult to test... but not impossible.

It is a well-established principle that among polygynous, harem-keeping animals, males are larger than females. Compare, for example, gorillas with gibbons. Gorillas establish harems, in which a dominant "silver-back" male mates with perhaps three to six females; male gorillas are two

26 the myth of monogamy

to three times larger than their mates, apparently because competition among males to be successful harem-keepers has conveyed an evolutionary advantage to those that are larger, stronger, and generally more effective in keeping their rivals at bay. By contrast, gibbons live in male-female pairs, so most healthy gibbons get to reproduce, even most males. As a result, there are very few big winners or big losers and, accordingly, virtually no size difference between the sexes.

Among monogamous species generally, males and females ostensibly have the same reproductive options. After all, when the female reproduces, so does the male, and vice versa. Such animals therefore shouldn't be sexually
dimorphic
(from the Greek for "two bodies"), because natural selection ought not to reward either sex for being overgrown, remarkably colored, or otherwise extravagant. But many animals long known to be socially monogamous are in fact sexually dimorphic, with males typically being more brightly colored than females--especially among birds. Consider mallard ducks, for example, in which the drakes have a dramatic, iridescent green head, whereas females are comparatively drab, or the many species of warblers in which, once again, males are extraordinary in their bright coloration, whereas the females are notoriously difficult to tell apart.

Darwin thought that perhaps dramatic male-female differences were maintained in such cases because more elaborately ornamented males got to breed earlier; as a rule, the early bird not only gets the worm, but he-- or she--also gets to have more successful offspring. So, one possible explanation for fancy secondary sexual traits among males in monogamous species is that for one reason or another, sexier males get to mate with more fecund females. A second possibility, raised only recently as the myth of monogamy bites the dust, is that sexier males are able to gain additional reproductive success through EPCs, at the expense of mated males that aren't as attractively adorned. Over time, this would increase the proportion of fancy-looking males or, at least, of males that are quite different from females of the same species. (This leads to an interesting, if troubling, possibility: As we shall see in Chapter 5, a powerful piece of evidence for the fact that human beings are biologically polygynous is the fact that men are generally larger than women. Although the evidence is still convincing in that direction, it is also possible that our own biological history was largely monogamous, with at least some male-female differences in
Homo sapiens
due to the fact that adultery figured importantly in that history.)

Back to the birds, where an important recent study focused on a small species known as the collared flycatcher, on the Swedish island of Gotland. It provides strong evidence that extra-pair copulations in this supposedly monogamous animal give certain males a distinct reproductive advantage. Collared flycatcher males have a white forehead patch; females don't. This

undermining the myth: males 27

patch is a secondary sexual characteristic. It also appears to be a status signal, whose size varies depending on its bearer's nutritional status as well as social success. Knowing the size of this patch, we can predict which collared flycatcher will win a territorial dispute between males. Moreover, if experimenters artificially increase the size of this patch, the fortunate males are more likely to establish a territory in the first place. Female collared flycatchers mated to males with large white forehead patches even produce a larger proportion of sons. This seemingly odd finding makes sense if males with prominent patches are likely to father sons with prominent patches. There would then be a reproductive payoff if such males father a comparatively large number of sons, which, in turn, will be relatively more successful than daughters ... who lack such distinguishing marks and, as females generally, are less likely to distinguish themselves reproductively.

The researchers found extra-pair paternity among collared flycatchers in 26 of 79 broods, accounting for 71 of 459 nestlings. After carefully analyzing their results, they concluded that "selection via variation in paternity"--- that is, some males having offspring via EPCs with females mated to other males--can be more important than "selection resulting from mate fecundity" (that is, more important than having greater numbers of offspring with their socially defined mates). Among collared flycatchers, in short, the major route to male reproductive distinction is not having more offspring with their "wives" but rather fathering offspring by various "lovers" who are already "married."

There have been many other studies along these lines, looking at species that are socially monogamous, most of them showing not only that males with highly developed secondary sexual traits have higher reproductive success but also that such success comes via EPCs. A typical one, in the prestigious journal
Nature,
was titled "Extra-Pair Paternity Results from Female Preference for High-Quality Males in the Blue Tit." Other studies have shown that male paternity--the proportion of offspring in his nest that are genetically his, as well as the number of offspring he will father in the nests of other males--is connected not only to the presence or absence of certain secondary sexual traits but also to the degree to which his secondary sexual characteristics are expressed.

Here are some notable examples: "DNA Fingerprinting Reveals Relation Between Tail Ornaments and Cuckoldry in Barn Swallows" showed that male barn swallows sporting more deeply forked tails are more likely to win the hearts of neighboring females. Another article, "Correlation Between Male Song Repertoire, Extra-Pair Paternity and Offspring Survival in the Great Reed Warbler," reported that in this European species--like barn swallows, ostensibly monogamous--males with a large variety of songs are also likely to have a variety of sexual partners. And don't overlook

28
THE MYTH OF MONOGAMY

this gem, potentially encouraging to any readers getting a bit long in the tooth: "Old, Colorful Male Yellowhammers,
Emberiza citrinella,
Benefit from Extra-Pair Copulations." Among these birds, males grow more colorful as they age. It appears that older, more colorful males therefore give promise of having a desirable set of longevity genes, which in turn are attractive to females. (Human beings, too, grow more colorful as they get older, and it is at least possible--if unlikely--that white hair has been selected as a similar symbol of status or, at least, of the ability to survive.)

It seems that the key dimension in these cases is female choice; since males of most species are unlikely to refuse a quick and easy EPC, the deciding vote as to who succeeds and who fails is generally cast by the females, based on whom they find most attractive. But the secondary sexual characteristics of males not only dictate their attractiveness to females, they also influence--and are influenced by--dominance relationships among males. And so, the two factors--dominance relationships and degree of secondary sexual traits--are confounded when it comes to determining which males obtain EPCs. Among cattle egrets, for example, the dominance standing among males has implications for who gets to have EPCs with whose mate. Dominant males have EPCs with the wives of subordinates but not vice versa. (This pattern is of course not unknown among
Homo sapiens,
too.)

On the other hand, one thing about biology--as compared with, say, chemistry or physics--is that there are lots of exceptions. This applies to the general correlation between male secondary sexual traits and reproductive success no less than to other generalizations (such as "animals eat plants but not vice versa," "only mammals are warm blooded," or "females are smaller than males"). There are, after all, insectivorous plants; it appears that dinosaurs were warm blooded, and among some species--such as jacanas, described earlier--females are larger than males. Similarly, male secondary sexual traits don't always correlate with reproductive success; that is, sexy males don't always get more EPCs, or--more important--they don't always get more EPFs (extra-pair fertilizations). Are these, like the examples of sex-role reversal described earlier, cases of exceptions "proving" the rule? It's too early to say.

It is clear that even in ostensibly monogamous species, males seek--and often obtain--EPCs. It is also clear that they do so at the expense of other males, namely, the ones "married" to those females who succumb to their charms. For an EPC-seeking male, the best arrangement is to father children with females who are already mated. In such cases (assuming the female is able to deceive her in-pair mate as to her infidelity and, thus, his nonpaternity), the female will gain paternal assistance from the cuckolded male, making it more likely that any offspring thereby conceived will be sue-

undermining the myth: males 29

cessful. At the same time, the extra-pair male receives this additional payoff: Since any resulting offspring will be reared by someone else, there is no additional parental effort required. Not only that but--at least in the case of birds--by having multiple sexual partners, extra-pair males literally succeed in placing their eggs in more than one basket. On the other hand, an EPC with an already-mated female is almost always riskier than one with an unmated female, since the outraged husband may find out and drive off an interloping male, possibly injuring him.

For the potential cuckold, therefore, an important option is to guard "his" female from gallivanting males, thereby possibly preventing them from achieving their aims.

(All this assumes, by the way, that the result of a successful EPC is that a mated female ends up bearing offspring sired by one or more extra-pair males and that, therefore, the in-pair male is the one who is victimized. But occasionally the in-pair female can be the loser: In one recorded instance, a mated male zebra finch succeeded in inseminating an unmated female, who then laid an egg in that male's nest. The result was one of the few documented cases in which, as a result of an EPC, the cuckolded party was a
female
--in whose nest the egg was laid--rather than a male. Most of the time, however, cuckolds are male, and for good reason: Among all species with internal fertilization--including birds, mammals, and reptiles--a female "knows" that any offspring emerging from her body is genetically hers, whereas a male has to take his mate's word for it, unless he is an especially assiduous mate-guarder.)