The Myth of Monogamy: Fidelity and Infidelity in Animals and People (9 page)

In any event, there are few things as sexually stimulating to socially monogamous animals as the possibility that the mated female might have had an EPC. Among orioles, males will copulate with their mates immedi-

undermining the myth: males 39

ately after hearing a recorded song from another oriole. One might say that in the oriole world, the song of a male is sexually arousing to other males; the evolutionary significance of this would be that the nearby song of another male suggests that someone might have recently copulated with the in-pair female. If so, paired males who are "turned on" by this telltale signal and who introduce their sperm as quickly as possible to compete with the extra-pair male would be favored by natural selection over those paired males who were indifferent to such cues.

David's research on mallard ducks has shown that males (especially unmated bachelors) will often "rape"--that is, force a copulation upon-- already-mated females. When this occurs, the mated male will typically respond by attempting to dislodge the attacker. Very quickly afterward, he forces a copulation with his own mate. Such behavior is not gentlemanly, but in the cold calculus of natural selection, it may be the best he can do to attempt to counteract the recent extra-pair mating.

The Galapagos hawk is unusual in that it is socially polyandrous: Up to five males will bond, socially and sexually, with one female. As soon as one male copulates with the female, the others quickly line up to do the same. It is not enough to say that sex, like laughing or yawning, is a "contagious" behavior. The best explanation for
why
it is contagious is that it signals the prospect of an extra-pair copulation and thus arouses an adaptive response, especially among males.

Mammals are not immune. Among rats, males mate with a female as quickly as possible after she has finished copulating with a prior male. Among nonhuman primates, males quickly mount and copulate with a female partner who has recently copulated with a different male. This implies that males are sexually aroused by indications that a female has recently copulated. And this, in turn, should not be very strange: Human beings, especially males, are also highly aroused by such indications. Hence, the attractions of hard-core pornography and voyeurism, which have been attributed to males generally having a low threshold for stimulation (since their investment in sperm is minimal).

This explanation is valid, as far as it goes, but it may not be complete. Thus, the adaptive significance of sperm competition may also be involved, since it would be adaptive for human males--no less than males of the other species we have mentioned--to be especially aroused by the prospect of sexual intercourse itself. This is even true if the sexual action is on the part of other individuals, if it indicates the nearby presence of a receptive female. Sperm competition would make it worthwhile for males to be prepared to join in, if possible, and to do so promptly, so as to compete with the preceding males. Moreover, the existence of sperm competition also helps explain a seemingly peculiar yet widespread aspect of human sexuality: Many

40
THE MYTH OF MONOGAMY

men are sexually aroused by thinking of their female partner having sexual relations with another male. Some even go out of their way to arrange such encounters (although this appears to be rare).

In at least one rat species, when a male has recently copulated with a female, the time interval before his next copulation with that same female is significantly reduced if, in the interim, he observes her copulating with another male. Most likely, by copulating promptly with a female who has recently copulated with another male, the "responding" male increases the chances that he, instead of his rival, will fertilize the eggs. Alternatively, he may simply diminish the chances of his rival(s) being successful, if there is direct interference among sperm produced by different males.

nd so, we come to an indelicate but revealing subject: testicle size.

Species in which mate-guarding predominates generally have small

JL
JL
testes; when frequent copulation is the preferred strategy, then, not surprisingly, the resulting male gonads are far more impressive.

For notable cases of frequent copulation, take those species that are polyandrous, in which one female regularly mates with more than one male (such as the jacanas, mentioned earlier). These animals typically have a high copulation frequency, probably initiated by males, each attempting to swamp the sperm of his rivals and thereby increase the chances that the eggs to be deposited in his nest--and which he will then incubate and care for-- are genetically his. The males of such species have oversized testes, producing more sperm than monogamous males whose responsibility is to inseminate their mate but not to compete with the sperm of other males. This pattern is not limited to birds. It has been found for mammals generally, confirmed by comparing, for example, rodent species that do and do not have many EPCs, as well as members of the horse family (including zebras) and even balleen whales. Ditto for primates.

As already mentioned, some bird species, including prairie chickens and sage grouse in North America, breed on what is called a "lek," a communal displaying ground. Males gather here and show their wares, calling and posturing and typically arranging themselves in a dominance pattern, with the alpha males in the middle. Females mate almost exclusively with these favored individuals, who may copulate with numerous females in one day; these females, in turn, generally give the subordinate males a cold shoulder. Systems of this sort provide the opportunity to answer this question: When males have especially large testes, is it because of sperm competition (that is, because other males are likely to be copulating with the same females) or simply because of the demands of producing enough sperm to fertilize the eggs of many different females?

undermining the myth: males 41

The answer iSS pretty clear: Whereas polyandrous species have large testes, the males of lekking species have testes that, corrected for overall body size, are if anything exceptionally
small.
Evidently, it is rather easy to make enough sperm to fertilize one female or even many, as dominant lekking males do.
What
really makes for big balls is when males must compete with the sperm produced by other males.

The most impressive case--or, at least, the one closest to home for readers of this book--comes from observations of the great apes. Remember those impressive silverback male gorillas, large in body and relatively aggressive in temperament, who succeed in dominating other males and gaining reproductive rights to a small harem of females? Although their bodies are large, their testicles are remarkably small, indeed downright tiny once corrected for body weight. By contrast, chimpanzee males--which do not achieve anything like the reproductive despotism enjoyed by their gorilla counterparts--have immense testicles. This is entirely reasonable, since a female chimp in heat will copulate with many different males; in one case, Jane Goodall observed a female chimpanzee copulate 84 times in eight days, with seven different males. As a result, a male chimp cannot simply assume that sexual access to an estrous female will result in paternity. He must produce enough sperm to give them--and thus, himself--a fighting chance. (When it comes to testicle size, human beings fall somewhere between the polygynous gorilla and the promiscuous chimp, suggesting that we are mildly polygynous. More--much more--on this later.)

Since testis size is largely influenced by sperm competition, not the simple need to inseminate a faithful partner, it is possible to use testis size as a rough measure of the sperm competition experienced by a species. In socially monogamous animals, there is much variability: Some species have relatively small testicles, suggesting very few EPCs. Others--especially those living in colonies--have large testicles: These include herons, sparrows, most seabirds, bank swallows and cliff swallows. In these cases, paired females have the opportunity to mate with other males. Of course, the same is true for males: They have the opportunity to mate with other females. But as we have just seen, it is unlikely that testis size is driven as much by the need to make lots of sperm in order to inseminate other females as by the need to compete with the sperm of other males. From this perspective, the female reproductive tract is an arena within which some pretty fierce sperm competition takes place. The tactics can be downright weird.

For example, it isn't even necessary to make large amounts of normal sperm, and in some cases males are better off if they don't, especially if sperm manufacture is relatively costly. Like an innkeeper trying to stretch his budget by watering down the drinks, males of some insects can induce a female to be sexually unreceptive to other males, at low cost to themselves,

42 the myth of monogamy

by introducing "cheap filler" into the females' seminal receptacles. Among certain species of
Drosophila
--fruit flies--males produce at least two different structural types of sperm, short ones and long ones. (The technical term is
sperm heteromorphism,
literally "different structures.") The assumption is that short sperm are cheaper to produce than long ones; this seems likely, since males producing short sperm mature earlier, suggesting that they have been using less metabolic resources. Although the shorties often constitute more than one-half the ejaculate, it appears that they do not directly fertilize eggs; their exact function is unknown, although the favored hypothesis is that the short sperm act as cheap filler within the female genital tract, making it less likely that a mated female will attempt to copulate again in the near future.

Among many insects, females are equipped with various organs that are specialized to receive sperm during copulation. Females will often remate when their sperm supply begins to wane. In some cases, it is simply the stretching effect, not some fancy pheromone, that does the trick, not unlike the hunger pangs that people feel when their stomach shrinks and the feeling of fullness and satiation that comes after eating, when the stomach is stretched. One researcher tried injecting silicone oil into the bursa copula-trix of a species of butterfly; in response, the females became not only distended, but sexually unreceptive. It is interesting to note that among butterflies, so-called apyrene sperm (those lacking genetic material altogether) are especially common, sometimes exceeding 90 percent of all sperm produced. It seems likely--although as yet unproven--that it is metabolically cheaper for males to produce these "blanks" than to outfit all their sperm with the full complement of DNA.

In the annals of sperm competition, an important consideration is whether there is an advantage in being the first to mate with a given female, or the last to mate, or whether all the sperm accumulate within a multiple-mating female, resulting in a "random lottery" with likely victory going to the male who contributes the most. Among insects and birds, the predominant pattern is "last male advantage," or "last in, first out." When sperm are accumulated inside the female in a specialized sperm storage organ (as in
Drosophila
or butterflies), it makes sense that the last sperm to have been added are likely to be the first squeezed out when her eggs finally pass by in reproductive procession. Like airline passengers waiting at a baggage carousel, whose luggage comes out sooner if it went in later, the last are likely to be first. Wlien it comes to the reproductive trafficking of some males, this has important implications for behavior.

Imagine that you are a male in one of these "last in, first out" species. Add to this the fact that ecological circumstances may dictate that you and your mate must spend considerable time apart. Not knowing for certain

undermining the myth: males 43

whether she has copulated with anyone else in the interim, your best strategy is to copulate often. That way, you increase the chances that yours will be the most recently deposited sperm--hence, the ones most likely to fertilize your mate's next egg.

All this assumes, of course, that the male and female have already made a reproductive commitment to each other--through courtship, building a nest, perhaps jointly defending a territory, and so on. In other cases, when EPCs loom large in evolution's strategic planning but the prospective pair have not yet decided to settle down together, there are alternatives to mate-guarding or copulating often. One of these is to refrain from making a commitment. For example, male ring doves behave aggressively toward females that reveal by their behavior that they have recently copulated with other males. The result is to delay the pairing, which is probably adaptive, since it means that by the time a male ring dove commits himself to a female with a colorful past, she will have already revealed that past by laying fertilized eggs. It is interesting that ring doves have an unusually short duration of sperm storage, so the suspicious male does not have long to wait.