The Myth of Monogamy: Fidelity and Infidelity in Animals and People (14 page)

So far, in examining the female search for sexual variety, we have looked at simple genetic success versus failure: producing offspring or failing to do so. This barely scratches the surface when it comes to reasons why females may elect to mate with more than one male. There are many aspects to mating "well."

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If females copulate with many different males, then in theory they can choose among the sperm of these various males and decide which one to favor with an egg or two, or, like an expert financial planner, they might even choose to diversify their genetic portfolio, allowing a preferred mix of different males to fertilize different numbers of their eggs--maybe even allotting certain eggs to certain sperm.

This may seem far-fetched, but it is not impossible. More plausible yet are a variety of EPC-related tactics by which females enhance the likelihood that their eggs will be combined with the best possible male genes. Imagine, for example, a female mated to a male via a long-term pair-bond. Imagine, further, that the male in question is something less than a sterling specimen: adequate, but nothing to write home about. Given the opportunity, in fact, the female would have chosen someone else. But since the species is generally "monogamous," she never had much opportunity to choose. After all, for every female there is, on average, one male, and vice versa. In a polygynous species, one male might be mated to a dozen or so females, in which case each of those 12 females might have been able to avail herself of the 1 in 12 males who is especially desirable, resulting in 12 happy females while also leaving on average 11 bachelor males. In such a case, their loss is the females' gain, since each harem-member has gotten an unusually high-quality mate--albeit the same one--who will presumably provide high-quality genes.

But in the case of our hypothetical monogamous situation, females have much less opportunity to choose a really classy male, since all the best ones have been taken, presumably by the best--most desirable--females. Furthermore, let's imagine that our monogamous female isn't such a prizewinner herself, so she wasn't exactly free to choose the male of her dreams. She had to "settle." Imagine, further, that her mate's sperm is good enough to fertilize all her eggs and to produce viable offspring. Still, it is one thing to be viable, another to be a raging success.

In order to reproduce at all, our female needed a social mate; otherwise, she wouldn't have a nest, for example, or a feeding territory, or the assistance of an adult male, necessary perhaps to defend her and her young or maybe to help provision the offspring. But recall that in obtaining these prerequisites--the material necessities of reproduction--she had to accept a male whose genetic traits are less than prepossessing. In evolutionary terms, it is not important that such a female may be "disappointed" or "dissatisfied" with her mate, except insofar as "disappointment" or "dissatisfaction" may be a human way of saying that she might be tempted to improve the genetic characteristics of her offspring by mating with one or more other males ... likely one of those desirable hunks with whom she was unable to establish a pair-bond.

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THE MYTH OF MONOGAMY

It is noteworthy that female animals only rarely have affairs with bachelors (who, after all, are likely to be rejects). Instead, they choose someone else's mate, probably because he offers better genes, plus--as we shall see in a bit--maybe other resources. Even harem-living females can sometimes exercise some control over their genetic partners. In species ranging from elephants to elephant seals, females seem to go out of their way to associate with a dominant male. They also vocalize loudly when a subordinate male attempts to mount them; this alerts other males to the copulatory attempt, whereupon the most dominant male is likely to drive away the subordinate interloper and mount the female himself. We cannot say whether the female "knows what she is doing," but it seems clear that, as a result, the lady elephant seal is more likely to be inseminated by a dominant male than by a subordinate.

Rather than directly granting sexual favors to one male in preference to others, female mate choice can thus be indirect. This might help explain why, in many species, females are inclined to aggregate at a mating site, from which a single dominant male can exclude other males. Or females can advertise, for example, that they are sexually receptive, thus generating conditions that provoke males to compete among themselves. The conspicuous estrous swellings of female primates may similarly have evolved in the service of indirect mate choice, with the Technicolor posteriors and yummy odors of estrous females inciting male-male competition, to the ultimate genetic benefit of the females.

Female garter snakes engage in a kind of
coitus interruptus
that apparently enables them to control who fertilizes their precious eggs. In eight of twelve observed copulations with unsuitable partners, females were seen to rotate their bodies wildly, interrupting the mating and preventing the formation of a copulatory plug. Dominant male red jungle fowl roosters (the wild forerunners of today's barnyard chickens) do not have to force females to copulate with them; only subordinate roosters must stoop to such behavior. Interestingly, of ten such forced copulations that were observed in one study, four were followed by vigorous feather shaking on the part of the female, which resulted in sperm being ejected from the cloaca.

Here is an anecdotal account of something equally thought-provoking in a common bird, the yellow warbler. It seems that on one occasion a particular male remained unmated throughout an entire breeding season, adopting instead the habit of forcing EPCs on "married" females. Once, after he forced such a copulation, his victim immediately flew to her mate and successfully solicited a copulation with him! In this case, a parsimonious interpretation is that the victimized female yellow warbler "preferred" to have her eggs fertilized by her social mate.

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Even without pushy males, females are often confronted with another sexual difficulty: a sampling problem. After all, they generally encounter males sequentially; that is, one at a time, perhaps with a fairly long pause in between. With each male they meet, they must "decide" (either consciously or not) whether to mate or wait, all the while not "knowing" whether they will encounter any others. Moreover, our female must somehow evaluate the breeding quality of each male, presumably either comparing him with some internal standard or against her memory of other males already encountered. One option--although not the only one--is to mate with the first male to come along, then mate again only if any subsequent swain shows himself to be better than the previous one.

It may be costly or even impossible for females to sample many different males before settling on a mate. For example, a female pied flycatcher visits on average only 3.8 males before choosing one. When females compete vigorously among themselves for a limited number of especially desirable males, their options may be even more restricted. As a result, females can hardly be expected to make a very informed choice; or, at least, their "choice" of a mate may be largely a matter of settling for whatever they can get. However we look at it, depending on how many additional males they encounter after they are paired up, some females may be likely to discover a male who is more desirable than the one with whom they find themselves. Under these conditions, "till death do us part" does not make a whole lot of sense. More likely is a strategy of "having your cake and eating it, too."

Think of it as a kind of one-way ratchet, whereby females, after accepting an initial mating, will mate again, but only if, by doing so, they are "ratcheting up," improving the genetic situation of their offspring. The tactic would be to mate with a seemingly good male--one who meets the minimum criteria of being of the right species, the right sex, and basically adequate--then remain available to mate with a better one, if he shows up. In a species of salamander, the European smooth newts, females pick up the sperm packets of males with particularly large head crests. In one experiment, females were exposed to males varying in the size of their crests, separated by 20 days. The females mated the first time, then had the choice of remating a second time or continuing to lay eggs fertilized by the sperm of their first mate. In this situation, most females only remated if the male to whom they were exposed the second time had a larger crest than the one whose sperm they had initially accepted. (Crestfallen, in such cases, is a severe condition indeed.)

In at least one species of spider, females that have already mated are willing to remate if they encounter a male with body size and fighting ability superior to that of their previous mate. Not only that, but the offspring of

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such multiple-mating females have a higher growth rate than those produced by single-mating females.

For any of several reasons, females can find themselves paired with males who are not genetically the best: As already mentioned, if the species is socially monogamous, only one female gets the best male. Everyone else is "settling." In territorial species, a female generally chooses a male based on the quality of his territory, although she may also use other criteria: whether he provides good parental care, or is especially adept at foraging, or is skilled at defending their young from predators. Alternatively, a female may simply settle on familiar real estate, taking the male who is there. Biologists have tended to think that life is a package deal: By getting, say, a resource-rich male, a female also gets the best genes. But this need not always be true. If a male who is genetically subpar ends up with a high-quality piece of real estate, he may also end up with a female who looks elsewhere when it comes to a sexual partner.

In nonterritorial species, where mates are chosen not for their resources but more often for their personal qualities, including their genetic attributes, EPCs may be less important. For example, among waterfowl such as ducks, pairing is based on individual traits, not on possession of real estate, and, significantly, female ducks are notable for how vigorously they resist attempted EPCs. It seems likely that in the duck world, most females are satisfied with the genetic makeup of their mates; hence, they are less inclined to copulate with anyone else.

In most vertebrates at least, females can control the timing of copulation, which in turn means that they can control fertilizations. The most common pattern in birds, for example, is for females to call the sexual shots: They initiate copulations and determine when to refrain. Surprisingly, perhaps, they stop copulating while the female is still fertile! At this time, they have obtained enough sperm to insure fertilization of their eggs but appear to be hedging their genetic bets, giving themselves the opportunity of "ratcheting up": If a better-quality male comes along, such a female has the option of copulating with him, too. Because of the "last male advantage" (last in, first out), this male is likely to fertilize more than his share. On the other hand, if no such desirable stud shows up, these females have lost nothing; their eggs will still be fertilized, this time by their social partner.

Another option---and probably a simpler one--is for the female to retain a memory of her last mate and choose a different one each time. This is the tactic followed by a strange little invertebrate known as a pseudoscorpion. In a well-designed research study, once-mated female pseudoscorpions were given the opportunity to mate with their earlier partner or a new male. After an interval of
IV2
hours, females invariably preferred new males, rejecting

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their previous mates; after 48 hours, on the other hand, they were equally likely to mate with their old lovers or with new ones. (The males were equally willing--indeed, eager--regardless of the interval.) This seems to be a way for females to increase their chance of acquiring a diverse array of sperm, while also making sure that they get enough tp fertilize their eggs. It had already been demonstrated that pseudoscorpion females--like female European adders--that mated with more than one male have more reproductive success than do females artificially restricted to mating with just one (that is, enforced monogamy). The key seems to be genetic incompatibility between some males and females rather than the intrinsic merit of a given male's sperm. It is less a matter of higher-versus lower-quality males than the "genetic fit" between any two would-be parents: The same male pseudo-scorpion may have highly successful offspring with one female but many "stillborn" offspring with a different female.

But in these animals, males don't appear to differ outwardly, even though each is genetically distinct. So females apparently cannot determine whether a given male is the one for them. Neither are pseudoscorpion females blessed with an especially good memory. Under these conditions, it may be that the best strategy for lady pseudoscorpions is to cast their reproductive nets widely, mating with new males rather than old partners and thus making it likely that at least one of their sexual consorts will provide the right, matching sperm. (Pseudoscorpions are wonderful little creatures, by the way. They reside under the bark of decaying tropical trees, and in order to leave one such tree and make their way to another they must hitch a ride underneath the wing covers of another small invertebrate, the harlequin beetle. Male pseudoscorpions compete with each other to monopolize the limited travel space; no carry-on luggage permitted.)