The Myth of Monogamy: Fidelity and Infidelity in Animals and People (5 page)

It is said that exceptions prove the rule. WTien it comes to the connection among maleness, low parental investment, and sexual eagerness, there are in fact some interesting apparent exceptions. These are cases of "reversed sex roles," in which females are comparatively aggressive, often larger, brightly colored, and more sexually demanding if not promiscuous, while the males are coy, drab, and sexually reticent. Among certain insects, for example, the males produce not only sperm but also a large mass of

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THE MYTH OF MONOGAMY

gelatinous, proteinaceous glop, which the female devours after mating; in doing so, she gains substantial calories, more, in some cases, than she expends in making eggs. And sure enough, in these species (including some katydids and butterflies), females court the males. This makes sense, since here it is the males, not the females, who make a large metabolic investment. And in such cases, males, not females, are likely to say "no." The key for our purposes--and apparently for these animals as well--is that male-female patterns of sexual behavior are reversed precisely when male-female patterns of parental investment are reversed. (It is not known, incidentally, what gave rise to such sex-role switching in the first place.)

Another lovely insect example of the exception confirming the rule comes from several species of fruit fly, including one known as
Drosophila bifurca.
The males, about 2.5 millimeters long, make sperm that are 20 times longer than the flies producing them! This would be the equivalent of a 6-foot man making sperm that are more than 120 feet long. The function of these giant
Drosophila
sperm is unknown (in some cases, the tail enters the egg at fertilization, in others it remains outside), but it is known that males, after constructing these remarkable devices, parcel them out "with female-like judiciousness, carefully partitioning their limited sperm among successive females."

Sex-role reversal has even been reported for some species of birds, notably the South American marsh-dwelling species known as jacanas. These animals are polyandrous, with a large, aggressive, dominant female maintaining a territory in which several small, meek, and subordinate males each construct a nest and incubate eggs that the dominant female bestows upon them, after mating. Because of their time spent nest-building and incubating, the male jacanas end up providing more parental investment than do the females ... and once again, the females act "male-like" in their sexual appetites, while the males behave more like females.

Of course, exceptions don't really prove rules; rather,
apparent
exceptions can help contribute to a rule if a more careful look shows that they aren't really exceptions after all. (Otherwise, exceptions
disprove
rules!) But when it comes to the correlation between low parental investment and high sexual appetite, this rule is pretty close to being proven.

By now, it should be easy to see why monogamy is under siege, at least from the male side. The potential reproductive benefit of having one or more additional sexual partners is high (if any of these "girlfriends" get pregnant), while metabolic and energy cost is likely to be low. Not surprisingly, males show numerous signs of this evolutionary pressure to stray from monogamy. One example is the so-called Coolidge effect.

undermining the myth: males 21

Legend has it that President Cal and his wife were separately touring a model farm. When the president reached the chicken-yard, containing a single rooster and several dozen hens, his guide said, "Mrs. Coolidge wanted me to point out to you that this one rooster must copulate many times per day." "Always with the same hen?" asked Coolidge. "No, sir," replied the guide. "Please point out
that
to Mrs. Coolidge!" the president responded.

The Coolidge effect is well known and has been confirmed in numerous laboratory studies: introduce, for example, a ram and a sexually receptive ewe and the two will likely copulate, typically more than once. The frequency then declines, usually quite rapidly. But replace the female with a new one, and the seemingly "spent" ram is--to some extent--sexually rein-vigorated. A new ewe makes for a new him.

Actually, this phenomenon was known long before the modern science of animal behavior. "I have put to stud an old horse who could not be controlled at the scent of mares," wrote the sixteenth-century essayist Montaigne. "Facility presently sated him toward his own mares: But toward strange ones, and the first one that passes by his pasture, he returns to his importunate neighings and his furious heats, as before."

As to human beings, listen to this account by a man from the African Kgatla tribe, describing his feelings about sexual intercourse with his two wives:

I find them both equally desirable, but when I have slept with one for three days, by the fourth day she has wearied me, and when I go to the other I find that I have greater passion; she seems more attractive than the first. But it is not really so, for when I return to the latter again there is the same renewed passion.

There is no reason to think that men inhabiting modern technological societies are any different. Indeed, the famous team of sex researchers led by Dr. Alfred Kinsey pointed out that

most males can immediately understand why most males want extramarital coitus. Although many of them refrain from engaging in such activity because they consider it morally unacceptable or socially undesirable, even such abstinent individuals can usually understand that sexual variety, new situations, and new partners might provide satisfactions which are no longer found in coitus which has been confined for some period of years to a single sexual partner... .On the other hand, many females find it difficult to understand why any male who is happily married should want to have coitus with any female other than his wife.

22 the myth of monogamy

About 80 percent of all mammal species are capable of multiple ejaculations, an ability that makes particular sense if these multiple ejaculations involve multiple sexual partners. In addition, although the Coolidge effect is very widespread, non-monogamous species (primates as well as rodents) show a stronger Coolidge effect than do monogamous species; this also was predicted, since males of non-monogamous species have more opportunity to act upon any sexual excitation they experience when they encounter a new female.

Most observers of animal behavior, not to mention observers of
Homo sapiens,
would agree that males generally have greater sexual urgency and lesser discrimination: Ask yourself, for example, is it men or women, who are accused of date rape, who engage in various sexual paraphilias ("perversions"), who visit prostitutes, and who have made pornography one of the largest industries worldwide? Once again, it makes biological sense for the sex that produces cheap, easily replaceable gametes to be readily "turned on" sexually and to be comparatively undiscriminating as to the target. (Thinking about it objectively, and without an evolutionary perspective, it is rather bizarre that huge numbers of men find it highly arousing to look at visual images of naked women! After all, these are merely dots of color on a page or, increasingly, a computer screen. Such people are not morons; intellectually, they know that these arousing images are just that--images--but the male tendency is to have an especially low threshold for sexual stimulation.)

What does an individual "get" from an EPC? For males, at least, it is obvious: sexual satisfaction. But this is what biologists call a "proximate" explanation. It may explain the immediate causation, but it leaves unanswered the deeper question:
Why
should sex--especially, perhaps, sex with someone new--be gratifying? The answer, for evolutionary biologists, is also obvious: Something is gratifying if it serves the biological interests of the individuals concerned. Such proximate satisfactions as "gratification" are evolution's way of getting creatures to do certain things. Or, more accurately, those who find such activities rewarding, and who therefore engage in them, leave more descendants who thus have similar inclinations. Hence, we find animals who seek food when hungry, rest when tired, warmth when cold ... and sex when horny.

Looking now at the evolutionary payoff of EPCs, it seems that males are unlikely to gain anything other than an increase in their reproductive success. After all, they have to expend time and energy seeking EPCs, and they may also be attacked by an outraged "husband." Moreover, since they are the eager ones and are providing only sperm--which, after all, are cheap-- it is unlikely that their female EPC partner will lavish "gifts" upon them, in the form of extra food, donated territory, assistance in defending their own

undermining the myth: males 23

offspring, and so forth. Whereas a mistress may gain material rewards from her lover (whether animal or human) in return for her sexual favors, a male out-of-pair sexual partner rarely is "paid" by his inamorata. For the male Lothario, the rewards are more likely to be immediate (the gratification of sexual dalliance itself) and long term (enhanced reproductive success), rather than material. For females, as we shall see in Chapters 3 and 4, the situation is quite different.

In any event, it requires no great conceptual leap to see how the low cost of sperm (and the resulting potential for a high reproductive rate) leads to a low threshold for sexual stimulation as well as a predisposition for multiple sexual partners; nor is it difficult to see how these, in turn, lead to a penchant for polygyny or, in cases of monogamy, to a susceptibility to EPCs. Either way, male biology bodes ill for monogamy. Interestingly, the biology of mammals is even more stacked against monogamy. This is because among birds, nestlings often have very high metabolic needs and therefore require the efforts of two committed parents. As a result, although male birds can often be expected to seek EPCs, they are somewhat less likely to maintain a harem of females. Not that male birds wouldn't happily attempt to accommodate such an arrangement; rather, their needy offspring are generally so demanding that most males are constrained to pitch in and, therefore, to have only a limited number of mates. But female mammals are uniquely equipped to nourish their offspring; indeed, mammary glands are what sets mammals apart from other animals. As a result, we can expect mammals to be even more predisposed than birds to form harems; that is, to be polygynous. And in fact they are. We already mentioned that monogamy is very rare among mammals. But we also mentioned the recent, dramatic discovery that even birds--including those that are socially monogamous--are much more prone to EPCs than anyone had imagined.

From an evolutionary perspective, copulations themselves don't really count; fertilizations do. And EPCs can be highly effective for males, whether bird, mammal, or any other species. Among red-winged blackbirds, more than 20 percent of a male's reproductive success comes from EPCs. Also, males having a high reproductive success with their own mates are likely to have high reproductive success via EPCs; in the world of reproduction, the rich get richer.

In fact, males who succeed in obtaining EPCs are in most cases already mated. This makes sense if the same underlying desirability of certain males that renders them more likely to obtain mates in the first place also contributes to their success when they go outside their mateships, seeking EPCs. But even here, there are exceptions. DNA profiling has recently allowed researchers to identify all the individuals, as well as all the offspring, of a small population of "stitchbirds," which are seemingly unremarkable little

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THE MYTH OF MONOGAMY

songsters except for this peculiarity: They copulate face-to-face, a position that may well be unique among birds. These animals were studied on an island off the coast of New Zealand, more precisely, Tiritiri Matangi. (For those readers who are geographically challenged, this will doubtless help: Tiritiri Matangi Island is about 3 kilometers off the Whangaparaoa Peninsula. Enough said.)

During the two breeding seasons in which the stitchbirds were studied, there was a heavy bias toward males in the population, a ratio of 3 to 1 in one year and 2 to 1 in the next. Nonetheless, social monogamy is the apparent goal of all self-respecting stitchbirds. But as a result of the unbalanced sex ratio, there were a large number of seemingly unsuccessful, bachelor males, so-called floaters. Thanks to a penchant for EPCs, however, these floaters were in no way reproductive losers: More than one-third of all nestlings were fathered by floaters (for another way of looking at it, 80 percent of all nests contained at least one extra-pair nestling). In fact, two of the unpaired floaters achieved more fertilizations than at least one paired male who played by the rules; this male had succeeded in pairing with a female in both years of the study, yet because of EPCs, his reproductive payoff was less than that of the two excluded floaters.

With findings like these, the importance of EPCs has become undeniable. It is also tempting to go further and conclude that males engaging in EPCs somehow experience a reproductive advantage over their IPC (in-pair copulation) counterparts. Accordingly, British biologist Tim Birkhead and his colleagues conducted an experiment to determine the effectiveness of EPCs in achieving fertilization. The subjects were zebra finches: small, brightly colored, socially monogamous birds native to Australia and commonly kept as pets throughout the world. In the wild, males guard their females before and during egg-laying, copulating about twelve times for each clutch. After allowing mated females to copulate on average nine times with their mated male, the experimental subjects were exposed to another male and allowed to copulate once. Both the mated female and the extra-pair male obliged. Wlien the researchers then used genetic plumage markers to determine paternity, they found, on average, that just one EPC yielded 54 percent of the offspring, compared to 46 percent paternity resulting from nine IPCs!