The Myth of Monogamy: Fidelity and Infidelity in Animals and People (8 page)

34 the myth of monogamy

the removed males were resisted by the females, who, it should be noted, continued to remain with their nest despite being made (albeit temporarily) into single parents. Similarly, extra-pair males that succeeded in copulating with the "visited" female were always in better body condition than the removed male. Not surprisingly, therefore, experimentally removed males that had been in poor body condition were more likely to wind up with "offspring" not their own. This suggests that the female has a lot to say about whether EPCs take place and, if they do, whether they are successful in actually fertilizing her eggs. (As we shall see, it also suggests what females are looking for when they engage in EPCs.)

It may well be that it is largely the females, not the males, who ultimately control the paternity of their offspring, although it seems that mate-guarding is an important factor. (If it weren't, then presumably males wouldn't bother doing it!) Among wheatears, at least, females were never seen behaving territorially toward intruding males; they allowed themselves to be visited and often courted, but they did not necessarily copulate with their extra-pair suitors.

Males can be extraordinarily crafty in setting up EPC opportunities for themselves, taking advantage of the preferences of females and, one way or another, getting around any efforts at mate-guarding on the part of in-pair males. Think about this series of events, observed among a species of gibbons living freely in the rain forests of Southeast Asia. Subadult males are tolerated within the family group, and perhaps not just because of paternal benevolence: In one case, while the male of a gibbon group was involved in an encounter with a subadult from another group, the adult male from the subadult's group rushed into the adjoining territory and achieved a copulation with the female! The possibility arises that adult males tolerate sub-adults in their group because the subadults occasionally get adjacent males socially entangled, giving the adult males an EPC opportunity.

More manipulating: In a series of observations of purple martins (birds related to swallows), it was found that older males monopolized several nestboxes and mated monogamously, one female to each male. Later, after that female was incubating--and thus was no longer fertile--the older males vocalized and thereby seemed to attract a following: Younger males set up housekeeping in the adjacent boxes. The older males then proceeded to obtain EPCs with the nubile mates of these less experienced, and presumably less attractive, young adults. As a result, the younger males fathered a mere 29 percent of the eggs
in their own nests,
whereas the older Casanovas produced, on average, 4.1 offspring via their female partner plus an additional 3.6 offspring via the mates of neighboring males.

(There may be a human parallel here, notably those charismatic men who establish cults or other forms of communal living arrangements and

undermining the myth: males 35

then proceed to monopolize the sexual attentions of the women, including those ostensibly associated with other, more junior cult members. Indeed, one of the main reasons for the failure of various
Utopian
communes has been eventual resistance to the sexual privileges typically demanded--and received--by the founding fathers.)

Males that are cuckolded are in double jeopardy: Not only are they more at risk of losing out genetically to gallivanters, but they are also less likely to be successful themselves in seeking their own EPCs. Why? Probably because those males especially likely to be cuckolded suffer this indignity because of some shortcoming in themselves. So whatever inclines their mates to seek matings elsewhere is also apt to make those same males unappealing to other females. They are losers two times over.

As a general rule, since the females of high-quality males are less likely to engage in EPCs, high-quality males have less need to guard. Older, more attractive males thus have a double advantage over their younger counterparts: Not only are they evidently appealing as sexual partners to already-mated females, but because they are so desirable, their own females are less likely to engage in EPCs. So these males have little need to spend time and effort mate-guarding and are therefore freed up to seek EPCs. The general pattern is concisely described in the title of one research article: "Unattractive Males Guard Their Mates More Closely." Several studies have confirmed that poor-quality males are generally more concerned with mate-guarding than are their high-quality counterparts, and for good reason, since females whose mates are less desirable are more inclined to seek EPCs. Males in poor condition are the Avis of Aves: They try harder.

And not only birds: It must be noted that among human beings, less attractive men invest more time and money in their mates than do men who are more attractive.

Aside from mate-guarding, how else can mated males diminish the threat posed by EPCs? In some cases, males have other anti-EPC tactics up their sleeves. For example, male swallows returning to their nests and finding their female absent typically give a loud alarm call, which causes all the birds in the colony to fly up in excitement. Several times this was seen to disrupt an EPC that the alarm caller's mate was engaged in. Maybe the husband was truly alarmed that his wife wasn't home. In any event, mated male swallows who experience this special kind of empty-nest syndrome are particularly likely to give alarm calls if they inhabit a crowded colony; faced with the same circumstances, solitary householders usually keep quiet.

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THE MYTH OF MONOGAMY

Males can also fit their mates with the equivalent of a chastity belt, a "copulatory plug." Among many species--including most mammals--part of the seminal fluid coagulates and forms a rubbery mass that is often visible, protruding slightly from the vagina. It used to be thought that these copulatory plugs served to prevent sperm from leaking out. And well they might. But it is increasingly clear that they also work the other way: to keep other males from getting in. It warrants repeating: Such devices would not be necessary if females weren't inclined to mate with more than one male.

In the world of spiders, males are often attracted by female pheromones, which waft downwind from their web. Not uncommonly, however, males will destroy a female's web after mating with her. Although not a chastity belt, such actions represents something similar: the male's effort to inhibit his mate's sexual activity. By ruining her web, the male drastically reduces the chances that another male will find and mate with the same female.

Please don't get the impression, incidentally, that females are merely passive bystanders or victims of all this sexual skulduggery. After all, in this chapter we are intentionally focusing on male strategies; in the next two, we concentrate on females. Biologist William Eberhard has been especially influential in pointing out the likely importance of what he calls "cryptic \ female choice," whereby females select which sperm will receive favored treatment and be admitted to their precious eggs. But insofar as females are exercising such choice, it is likely that males will try to horn into the act, each attempting to bias the outcome in his favor. Eberhard reviewed the sweaty details of what male insects actually do during courtship and copulation in 131 different species; he found that 81 percent showed behavior during copulation that he considered to be "copulatory courtship," activities that go beyond the simple necessities of transferring sperm and that appear to be directed toward persuading females to transfer and retain
their
sperm, in preference to the sexual products of other males.

Another possible male response to the EPC threat is frequent copulation. In mate-guarding, a male uses his body to keep other males at bay; by relying on frequent copulation, he uses his sperm... lots of them, delivered
_/
often. The idea is simply to overwhelm the opposition, to swamp their sperm with one's own.

Of the two tactics, it seems likely that mate-guarding is more efficient; after all, successful mate-guarding means there is essentially no chance of being cuckolded, whereas frequent copulation simply invokes probability, attempting to tip the genetic scales in one's favor. Also, even though sperm are cheap compared to eggs, they are not free. Just as males who defend their genetic patrimony by mate-guarding are unable to simultaneously seek their own EPCs, those who employ frequent copulation may limit the

undermining the myth: males 37

amount of sperm they have available for gallivanting. Even the most super-stud males, after all, cannot produce unlimited amounts of sperm or semen. Because of their basic biology, they can be more profligate than females, but only within limits; to a degree, they, too, must be prudent. Hence, by giving themselves an advantage in sperm competition with their mates, such males might be placing themselves at a disadvantage when it comes to sperm competition for someone else's mate. Sure enough, when male rats, for example, are given the opportunity of mate-guarding, they deliver fewer sperm per ejaculation. So it may be that mate-guarding is doubly preferred, both to seeking EPCs and also to sperm competition.

Sometimes, however, males have little choice: Females mate with more than one male and cannot be prevented from doing so. What is such a male to do? In one particular species of zebra--known as Grevy's zebra, for its discoverer--individuals live in groups whose membership is constantly shifting. Females associated with a given male are likely to mate with a different male not long afterward. In fact, during a single day they may mate with an average of four different males. (Call these females polyandrous.) On the other hand, there are some Grevy's females--generally, those who have just given birth--who remain with one male for a prolonged period, during which they are essentially monogamous. They do this, by the way, because they need reliable sources of water, which are found only on a male's territory. So Grevy's stallions have two different kinds of females to deal with, those that are sexually faithful and those that aren't (bearing in mind that the same female will occupy different roles at different times in her life).

Grevy stallions adjust their tactics accordingly, depending on whether their female consort is polyandrous or monogamous. When mating with polyandrous females, males invest more time and energy in mating itself: Stallions call to and copulate seven times more frequently than when involved (temporarily) with monogamous females. They even ejaculate larger quantities of semen. It is also worth noting that in another zebra species, the plains zebra, females live in traditional harems, each led by single male, and as far as is known, they only mate with the harem-keeper. Plains zebra stallions copulate less, produce less semen, and also have smaller testes than their Grevy's counterparts, which have to be prepared to deal with females having an occasional penchant for a high-frequency of EPCs.

Grevy's zebras do not mate-guard; instead, the stallions are prepared to engage in sperm competition when need be. This raises new questions. Why rely on one strategy rather than another? Specifically, why don't all animals mate-guard, since that seems more efficient? (And also, what about human beings, who are not shrinking violets when it comes to mate-guarding but who also copulate far more frequently than is needed for reproduction

38 the myth of monogamy

alone?) The answer seems to be that in most cases mate-guarding is the primary strategy, with frequent copulation being the next-best alternative, resorted to when males and females must spend substantial time apart. This occurs, for example, among predatory birds; one individual often remains by the nest while the other goes on lengthy hunting excursions. Not surprisingly, predatory birds copulate a lot.

Take ospreys. These "fish-hawks" are large predators, the males of which provide virtually all the food while their mates are occupied with nest-site duties. Hence, male ospreys are unable to guard their females; they are too busy fishing. Female ospreys remain invisibly chained to the nest from the time they arrive in the spring until their young are independent, at about three months of age. Observations at several osprey nests reveal that pairs copulate frequently, on average 59 times per clutch, beginning when the female arrives on the territory. Males are absent about 30 to 50 percent of daylight hours, which provides opportunity for female EPCs as well as the motivation for paired males to insist on frequent copulations when they are back at home after a long day's fishing.

In the case of purple martins, we saw older males using EPCs to take reproductive advantage of younger, inexperienced males. In other species, males are likely to obtain EPCs from females who are poorly provisioned by their mates. This has been especially well established among our friends the ospreys. So, not only does a hardworking male osprey run the risk that his mate will "take a lover" while he is away looking for food, but that risk is intensified if he is no great shakes at bringing home the salmon. It is not known whether male ospreys that are particularly inept as providers try to make up for this by copulating even more often than is the osprey norm.

It is well known, however, that among many different species, a resident pair is especially likely to copulate just after an intrusion into the pair's territory. It appears--although it is not yet proven--that this response to intruders is initiated by the in-pair male. This would make biological sense, since intruding males in such cases are unlikely to have simply dropped by to borrow a cup of sugar or to sell Girl Scout cookies. Why should the female go along with this, agreeing to copulate with her mate just because some other male has recently been hanging around? Perhaps it is simply less costly for her to acquiesce than to resist her mate's importunities. Or it may pay her to permit copulations--especially when her fidelity is in question-- so as to persuade her mate of his paternity, in order to assure his assistance in rearing the young. (As we shall see, the loss of paternal assistance is a major potential cost to females of EPCs, if discovered by the in-pair male.)