The Myth of Monogamy: Fidelity and Infidelity in Animals and People (7 page)

Let's take a brief excursion to a cattle pasture, almost anywhere in the world. One common occupant--far more numerous than the cows--is a tiny insect, the yellow dungfly. Male dungflies gather around cowpatties, especially the fresh ones, where they search for females who are about to lay their eggs in the warm, gooey interiors. Interestingly, these arriving females have nearly always copulated
before
arriving at the egg-deposition sites. Therefore, they already contain enough sperm in their genital storage organs to fertilize all their eggs. Yet before ovipositing, they copulate once again with at least one waiting male. Why?

The answer seems to be that among dungflies, the last male to mate guards "his" female until she is finished laying her eggs. Having such a protector greatly reduces the harassment that a female would otherwise receive from other males. This isn't a bad deal for males, either, since they experience a "last male advantage": The last male to mate fertilizes more than 80 percent of a female's eggs. Guarding takes about a quarter of an hour, which is probably a good trade-off.

Guarding doesn't always work, though. If another male dungfly, much larger than the guarder, attacks the pair, he may succeed in copulating yet again with the female, after which he proceeds to stand guard himself.

30 the myth of monogamy

Mate-guarding is very widespread. It is even possible that the well-known tendencies for animals of many different species to establish and defend territories is really a consequence of males guarding the sexual rights to their mates by defending a region surrounding them. In a sense, mate-guarding is one of the clearest animal (or human) manifestations of sexual jealousy, and it is sometimes quite overt, with the male shadowing every movement of his mate. Such "togetherness" is almost certainly not a simple--or even complex!--matter of love or loneliness, since it is nearly always limited to precise times when the female in question is fertile. Male bank swallows, for example, closely follow their mates, flying along nearby whenever they venture from their nests; such devoted attention quickly terminates, however, when the females are no longer fertile.

Mate-guarding is also a common male strategy among mammals, especially when the female is in estrus. The goal, once again, is evidently to thwart EPCs. Mate-guarding is also widespread, almost universal, among that mammalian species known as
Homo sapiens:
A now-classic anthropological review recorded that only 4 out of 849 human societies did not show some signs of mate-guarding, whereby men keep close tabs on their mates. In some societies, husbands even time their wives' absences while they are in the bushes urinating or defecating. Such concern may not be ill founded; one piece of British research found that the less time a woman spent with her primary mate (husband or identified main sexual partner), the more likely she was to have copulated with someone else.

We used to think that the close association of male and female, especially in a monogamous species, was simply a manifestation of their close pairbond, as well as perhaps a way of further enhancing their relationship. Here is a description of courtship among European blackbirds, from a classic 1933 account by ornithologist E. Selous:

The male bird follows her all about, hopping where she hops, prying where she pries, and seeming to make a point of doing all she

does except actually collect material for the nest____Then, the one

laden, the other empty-billed, they both fly back in just the same way, and the cock will sit again ... for the cock is as busy in escorting and observing the hen as she is in collecting material for building the nest.

Today: same observation, different interpretation. The male's observing and escorting seem motivated less by love or chivalry than by sexual jealousy and the specter of EPCs. The relationship of mate-guarding to EPCs is complex, and expected to be. On the one hand, we might anticipate a negative relationship: the more mate-guarding, the fewer EPCs. This seems the most obvious connection. But on the other hand, if EPCs are rare occur-

undermining the myth: males 31

rences in a particular species, then we wouldn't expect males to waste a lot of their time defending against such a nonexistent threat. There is in fact quite a range out there in the natural world, from essentially no correlation between mate-guarding and EPCs, to a positive association, to a negative one. (The determining factor may well be where each population is being sampled in its evolutionary history: If there is a continuing arms race between males seeking EPCs and those seeking to prevent them, then it might see-saw back and forth, with one side or the other ahead in different species at different times.)

As we now understand it, mate-guarding can take many forms, with-- not surprisingly--some of the more bizarre patterns revealed by insects. Among numerous species of bees, for example, the lower abdomen of the male almost literally explodes after mating, part of it then adhering to the female and thereby providing a kind of posthumous mate-guarding. Among a group of insects known as phasmids, genital contact during mating can last as long as 79 days; this tantric excess can be seen as an extreme example of mate guarding.

The widespread male preoccupation with mate-guarding fits our expectations of something motivated by the threat of EPCs. Thus, it is typically more intense with increased risk of the female's engaging in an EPC. Among barn swallows, which nest both solitarily and in colonies, females are guarded more closely in the latter case (when the proximity of numerous males makes EPCs more likely) than in the former (when there are no sexual competitors nearby).

On the other hand, for all its logic, mate-guarding presents us--and the mate-guarders--with an interesting irony. It wouldn't be needed if males themselves were not gallivanting about, seeking EPCs. If no one gallivanted, no one would have to mate-guard, Moreover, mate-guarders themselves, when not on guard, are likely to be out gallivanting! In fact, it may well be that the major constraint against doing yet more gallivanting is that while off seeking EPCs, a gallivanting male may find himself cuckolded... by another gallivanting male!

Recall those male bank swallows who so attentively fly after their females. Male bank swallows are socially monogamous and assist their mates in building the nest and incubating and feeding the young. In addition, they regularly seek EPCs with other females, before and after pair-bonding. Accordingly, they gallivant about in search of EPCs and also guard their mates against other gallivanting males, but, of course, they can't do both simultaneously. For seven to nine days after pair-formation, the male pursues the female whenever she flies from her nest burrow--up to 100 times per day. Other males seek to make contact with the female during these flights; in fact, the labored, heavy flight of a female carrying unlaid eggs may

32
THE MYTH OF MONOGAMY

serve as a cue to the other gallivanters. For his part, the guarding male actively seeks to drive the female back to the home burrow, especially when she flies into heavy traffic and may be pursued by three or four bank swallow males, starry-eyed with visions of a quick EPC.

For about four days immediately prior to egg-laying, when copulations lead to fertilizations, the male bank swallow is very busy, attentively guarding his female. Before this time, as well as after--that is, when her eggs are not ripe, and again after his genes are safely tucked away inside the shells-- he goes seeking EPCs with the mates of other males ... who, of course, are busy with defensive mate-guarding of their own.

It is unlikely that these chases are "sexual displays," intended to enhance the pair-bond, as earlier literature in animal behavior had suggested. This is because (1) males always chase females, not vice versa; (2) males typically fight with other males as an immediate result of such chases; and (3) when their own female is no longer fertile, mated males typically join in chases of other females, even though bank swallows are strictly monogamous, at least at the social level. Thus, such males could not be solidifying an additional pair-bond, if only because no such "double-bonded" males have ever been found.

David has traced a comparable pattern of mate-guarding and gallivanting among hoary marmots, social-living, mountain-dwelling relatives of the eastern woodchuck. The male makes periodic forays beyond his colony area, apparently in search of EPCs with fertilizable females. These episodes are significantly more frequent early in the season, when females are in estrus. Alternatively, a male marmot sometimes remains close to his female, guarding her from other sexually motivated males. It is clear that this passion for togetherness is initiated by the male, not the female, since during times of guarding, physical proximity is maintained by his movements, not hers. Furthermore, males are more likely to gallivant when their female is within her burrow, rather than out in the mountain meadows, and also when their neighbors are predominantly adult females rather than adult males. When the opposite condition holds--lots of other males nearby-- mated males, not surprisingly, concentrate on guarding. Females of this species breed in alternate years; as expected, males that are associated with nonbreeding females go gallivanting, whereas during the season that his female is reproductive, the male stays at home, mate-guarding.

The evolutionary benefit of mate-guarding depends on how many other males are doing the same thing: If everyone else is staying home and mate-guarding, a would-be gallivanter wouldn't have to worry that while he was out seeking EPCs, he might be cuckolded by other EPC-seeking males. But at the same time, the more mate-guarding he does, the less likely our male is to achieve his sought-for EPC. Lots of other gallivanters means a greater chance of being cuckolded, but also a greater chance of gaining access to

undermining the myth: males 33

someone else's unguarded females. No one said that these things were going to be easy! The best way to understand such complex trade-offs is through the mathematics of game theory, which is concerned with examining interactions for which the payoff depends on what other "players" are doing. Although this is not the place to develop such an analysis, it is a good place to point out that, in a very real sense, the dilemma of EPCs versus mate-guarding is one of the males' own making (with a little help from the females).

When males are mate-guarding, they rarely gallivant. This suggests that the former has priority over the latter, which makes sense since the prospects are usually better of preventing an outsider from copulating with your own mate than of obtaining an EPC with someone else's. But when that mate is no longer fertile, all bets are off; at this point, males typically switch to gallivanting. For example, consider rock ptarmigans, partridge-like birds of the arctic-alpine regions. Wlien the females are fertile, males average one intrusion onto a neighbor's territory every 14 hours. As soon as their mates are infertile, however, male intrusion rate jumps to one intrusion about every 1.4 hours, a 10-fold increase. And you can bet that those intrusions are not simply intended to exchange pleasantries or talk about the weather.

new cottage industry has sprouted among field biologists. In addi-

tion to using DNA fingerprinting to find out whether the "hus-

-i-
JL
band" of a seemingly monogamous pair is also the father, interest in EPCs and mate-guarding has given rise to a slew of research studies in which males are live-trapped and kept away from their mates for various periods of time. The intent is to see whether extra-pair males take the opportunity to "make a move" on the temporarily abandoned females. If so, this suggests that mate-guarding is normally important in the species. Just about always, it is.

For example, when male wheatears (small, monogamous birds) were removed for 24 hours during the female's fertile period, the frequency of intrusions by neighboring males and the number of EPCs shot up. By contrast, when males were removed during incubation (a time when females are no longer capable of being fertilized), there was no such increase. Extra-pair males are evidently able to determine whether a temporarily single female is likely to be sexually receptive. Not surprisingly, extra-pair paternity was higher (by about 25 percent) when the paired male was experimentally removed.

What characterized successful intruding males? In addition to the secondary sexual traits already mentioned, the key seemed to be the body condition (weight, overall health) of the intruders relative to the mated males that had been removed. Extra-pair males that were in poorer condition than