The Myth of Monogamy: Fidelity and Infidelity in Animals and People (13 page)

Broadly speaking, there are two kinds of benefits females can gain by mating with someone other than their identified partner. They can profit indirectly, via superior offspring fathered because of the EPC, or they can profit directly, gaining material benefits for themselves as well as their descendants. In this chapter, we'll examine the genetic or indirect benefits; in the next, we turn elsewhere.

One possibility--the simplest--is fertility insurance. To be sure, males produce millions, often hundreds of millions, of sperm in a single ejaculation, whereas, in most species, females release no more than

SO
THE MYTH OF MONOGAMY

a handful of eggs at a time. Just as the Marines used to advertise that they were looking for "a few good men," it seems likely that females, looking for a few good sperm, should have very litde difficulty, since sperm are available to fertilize eggs in a ratio of millions to one.

Granted, it only takes one "good" sperm to penetrate an egg. Yet for reasons that are not clearly understood, it appears that there must be millions of willing and able pollywogs nearby in order for fertilization to be reliable. Among human beings, for example, if a man produces "only" 50 million sperm per ejaculation, he is generally considered sterile. In addition to sheer numbers, sperm must also be "viable," which means able to swim upstream--and quickly. Moreover, when they arrive at the Holy Grail of their journey--a ripe and willing egg--sperm have to be sporting the right kind of protein coat surrounding compatible genes. The upshot is that females who copulate with several different partners are more likely to get all their eggs fertilized; this has been found to be true for fruit flies as well as birds.

Female cormorants are more likely to engage in EPCs when they have produced relatively small broods. It is possible, of course, that EPC-prone females have fewer offspring
because
they have indulged in EPCs, but more likely that they have EPCs because they would otherwise have fewer offspring. This is suggested by the fact that females who failed to fledge chicks were those that subsequently engaged in most of the EPCs. Further evidence comes from a study of house sparrow nests, which found that nests containing infertile eggs are significantly more likely to contain an EPC-fathered chick than are those lacking infertile eggs. Females consistently have more EPCs when their breeding success is otherwise low, suggesting that it is not simply a matter of some females being particularly inclined to mate outside their social union.

Among those birds whose females are genetically rewarded for multiple matings are, interestingly, red-winged blackbirds, the same species that had so startled the ornithological world more than 25 years ago when females mated to sterilized males were found to have reproduced. Although the effect is not dramatic, it is nonetheless real: Female red-wings who "play around" lay more eggs and enjoy a higher hatching rate than those who remain sexually faithful to one mate. Moreover, their peak of EPCs occurs one day
closer
to egg-laying--when their fertility is higher--than the peak of IPCs (intra-pair copulations). Since there is no evidence that such females are being raped or coerced in other ways, the conclusion seems unavoidable: Female red-wings are timing their EPCs to maximize fertilizations (we'll see later that there is some evidence that human beings--probably unknown to themselves--do the same thing).

Although, under natural conditions, very few red-wing males are permanently sterile, many are evidently subpar at least temporarily when it

undermining the myth: females (choosing male genes)
61

comes to producing successful sperm (more than 10 percent of eggs do not hatch). Interestingly, the number of eggs failing to hatch is positively correlated with the number of females socially mated to a given male; a likely possibility is that with many females to fertilize, the sperm production of some males is unable to keep up with demand. As a result, females may "demand" to copulate with other males. (The problem of sperm depletion is not altogether unknown to human beings: Couples complaining of infertility are typically counseled to
reduce
their frequency of intercourse, since an overactive sex life can diminish a man's sperm count to the degree that it interferes with fertility.)

Strangely, female red-wings do not seem to prefer better-quality males; at least, they do not solicit EPCs from males that had the highest reproductive success the previous year. There is still much for us to learn about this business!

The red-winged blackbird population described above was studied in central Washington State. Although their situation does not seem unique, it may be misleading to generalize too readily to other populations, not to mention extrapolating to other species. Thus, although Washington State female red-wings initiate EPCs, in another closely monitored population, in New York State, female red-wings only accept or resist the advances of males. They do not initiate.

Although it seems likely that natural selection would provide males with the ability to make enough sperm, it is nonetheless possible that EPCs provide females with a kind of "sperm security," just in case their mate's supply is running low. Extra-pair copulations are frequent among house sparrows, and especially so among those that produce infertile eggs, suggesting that when females are mated to infertile males, they are more likely to seek EPCs. At this point, it isn't at all clear how a female can ascertain the sperm supply of her male partner.

It is possible that they can't, in which case it may pay them to mate with more than one male, just for insurance. Among Gunnison's prairie dogs, female do just that. It turns out that the rare Gunnison's female who copulates with only one male has a 92 percent probability of becoming pregnant and giving birth, while the probability is 100 percent for females that copulate with three or more different males. In addition, litter size is larger when the number of sexual partners is higher. Not all mammals show this pattern, however, including even some other ground squirrels, which are closely related to prairie dogs. In fact, even in another prairie dog species, the black-tailed prairie dog, there is no such tendency. In some mammals, there is actually a
reduction
in female reproductive success associated with mating with a second male, at least under laboratory conditions. But maybe this last finding isn't so contradictory after all: It makes sense that a female might fail

62
the myth of monogamy

to conceive in the presence of more than one male, whereas she might do just fine if she had the chance to consort with one male at a time, privately, and on her own terms.

Throughout most of the animal world, females have something that males want: their eggs. And nearly always, males are quite willing-- even eager--to provide sperm. As a result, females are unlikely to be so desperate for sperm donors that they cannot exercise a degree of choice. This is in fact a useful way to look at the phenomenon of EPCs: They provide females with additional opportunities for choice, selecting a
genetic
partner independent--if need be--of their
social
partner.

Not surprisingly, females are less likely to face the question of "to fertilize or not to fertilize" than "to fertilize well, or not." According to legend, Cleopatra--not known for sexual abstention--was killed by an adder, a species of snake, which, it now appears, is no more monogamous than the famous queen herself. Thus, in a paper titled "Why Do Female Adders Copulate So Frequently?", a group of researchers reported that in at least one kind of adder, females that mate with several different males have fewer stillborn offspring than do their unlucky counterparts who are forced to mate with one or just a few partners. In such cases, the key contribution distinguishing one male from another seems to be whether his genes lead to healthy development after fertilization. There is a lot that can go wrong in the journey from fertilized egg to fully formed little snakelet. The more males a female adder mates with, the more likely she is to encounter a partner whose sperm will complement her own, leading to increased success in successfully negotiating the pitfalls of snake embryology.

This is as good a place as any to confront a possible misunderstanding, one that might otherwise bedevil many readers, here and elsewhere. Thus, some of you may balk at the notion of animals choosing their sexual partners with such exquisite care. You may feel tempted to throw this book across the room, exclaiming in frustration: "Wliat are you talking about? How could female adders possibly know so much--indeed, anything at all!--about the precise pitfalls of their own embryology?" As a matter of fact, even well-trained biologists don't know a whole lot about snake embryology. The point is that living things have evolved the ability to engage in all sorts of activities without necessarily having any detailed understanding whatever about what they are doing or why. Flowers bloom in the spring without "knowing" that their seeds will be most successful as a result, because they will germinate in the summer. Animals--including human beings--engage in an extraordinary array of fancy biochemical, molecular,

undermining the myth: females (choosing male genes)
63

and electrical events (think of digestion, respiration, DNA transcription and translation, the immune response, indeed, even thinking itself) without consciously understanding either the general processes or the details.

So please don't get "hung up" on such details yourself, at least as they pertain to the ability of living things to behave adaptively, just as they grow and metabolize adaptively even if they have never read a textbook, attended a lecture, or conducted a single laboratory experiment!

We hope you can grant, then, that a female's motivation in obtaining one or more EPCs might well go beyond fertility insurance to include an unconscious, evolutionarily based search for "complementary" genes. But what, specifically, might such a female be seeking? Based on theory alone, it would seem that copulating with more than one male would not convey a benefit in terms of added genetic diversity, since part of the charm of gamete production is the generation of astronomical genetic diversity; the genetic variety per se within just one male's ejaculation is immense, offering nearly as much range as can be obtained by mating with several different males.

On the other hand, there are often substantial costs associated with inbreeding, the mating of close relatives. Physical deformities are common, for example, among the offspring of closely related European sand lizards. DNA fingerprinting has shown that when a female sand lizard mates with a closely related male, he is likely to sire a small proportion of the offspring produced; more distantly related ("outbred") males father a larger proportion of the young. By multiple mating, a questing female seems likely to increase the chance that she will find a partner who is genetically different from herself.

This is not just a reptile thing. In a bird species wonderfully called the splendid fairy-wren, a high frequency of EPCs is apparently due at least in part to the benefits of avoiding inbreeding. And mammals are not immune to such considerations. A group of genes known as the major histocom-patability complex (MHC) serves as a key marker by which the immune system distinguishes "self" from "other." It also serves to indicate genetic closeness and is important in producing viable offspring. Among mice, offspring with incompatible MHC genes are spontaneously aborted. Interestingly, when female mice find themselves occupying the territories of males whose MHC genes are incompatible with their own, these females engage in EPCs with males from adjoining territories, whose MHC genes are a better match. (It appears that different MHC genes produce different odors, to which the females are sensitive.)

Female primates, for their part, often show a particular interest in mating with a male who is the new guy on the block. Paradoxically, although these new arrivals are nearly always low in social rank, they are often

64
the myth of monogamy

sexually appealing to females. For example, in one troop of Japanese macaques, a newly arrived male occupied the lowest social rank but mated with more different females than any other male. In one remarkable case, a female red howler monkey consistently turned down the local boys but was receptive any time she encountered a male from a neighboring troop.

The human equivalent--if any--isn't clear, but one hint may come from the interest and even fascination often generated by the "drifter," the mysterious newcomer. Even the cliche "You will meet a tall, dark stranger" might also capture some of the (literal) romance of novelty. On an evolutionary level, it is at least possible that this "strange-male preference" derives from inbreeding avoidance. In which case, it isn't so strange after all.

A key summary point is that in a wide range of species, females exercise direct choice as to their sexual partners, often choosing more than one. Although such behavior may prove risky for females if they are punished by their cuckolded male consort, when successful they could be repaid by bestowing the benefits of outbreeding upon their offspring.

Don't be too quick, however, to conclude that EPCs always pay for themselves via outbreeding. There are, it appears, different strokes for different species: Just as there is a downside to too much inbreeding, excessive outbreeding, too, can carry costs. In at least one case, EPCs seem, paradoxically, to be a mechanism for keeping genes
in
the family instead of introducing new ones. In one bird species, the pied flycatcher, breeding pairs that are genetically quite different are more likely to have extra-pair young in their nests than are those who are genetically more similar. In this species, therefore, it appears that females are prone to mitigate the effects of extreme outbreeding, seeking EPCs with males who are somewhat more genetically
similar
to themselves. The problem with excessive outbreeding is that it might break up locally adapted gene combinations, which simply means that by combining individuals who are too different, the resulting offspring might fall between two stools, landing on neither. Females may well choose as mates those likely to meet the Goldlilocks criterion: a partner who is not too similar, and not too different, but Just Right. (It is also possible, incidentally, that when a male and female pied flycatcher are just "too different" genetically, they are somewhat behaviorally incompatible as well, which would lead directly to more EPCs.)