Why Evolution Is True (27 page)

The theory of why the two sexes have different numbers and sizes of gametes is equally messy. This condition presumably evolved from that in earlier sexually reproducing species in which the two sexes had gametes of equal size. Theoreticians have shown rather convincingly that natural selection will favor changing this ancestral state into a state in which one sex (the one we call “male”) makes a lot of small gametes—sperm or pollen—and the other (“female”) makes fewer but larger gametes, known as eggs.

It’s this asymmetry in the size of gametes that sets the stage for all of sexual selection, for it causes the two sexes to evolve different mating strategies. Take males. A male can produce large quantities of sperm, and so can potentially father a huge number of offspring, limited only by the number of females he can attract and the competitive ability of his sperm. Things are different for females. Eggs are expensive and limited in number, and if a female mates many times over a short period, she does little—if anything—to increase her number of offspring.

A vivid demonstration of this difference can be seen by looking up the record number of children sired by a human female versus a male. If you were to guess the maximum number of children that a woman could produce in a lifetime, you might say around fifteen. Guess again. The
Guinness Book of World Records
gives the “official” record number of children for a woman as sixty-nine, produced by an eighteenth-century Russian peasant. In twenty-seven pregnancies between 1725 and 1745, she had sixteen pairs of twins, seven sets of triplets, and four sets of quadruplets. (She presumably had some physiological or genetic predisposition to multiple births.) One weeps for this belabored woman, but her record is far surpassed by that of a male, one Mulai Ismail (1646-1727), an emperor of Morocco. Ismail was reported by
Guinness
as having fathered “at least 342 daughters and 525 sons, and by 1721 he was reputed to have 700 male descendants.” Even at these extremes, then, males outstrip females more than tenfold.

The evolutionary difference between males and females is a matter of differential
investment
—investment in expensive eggs versus cheap sperm, investment in pregnancy (when females retain and nourish the fertilized eggs), and investment in parental care in the many species in which females alone raise the young. For males, mating is cheap; for females it’s expensive. For males, a mating costs only a small dose of sperm; for females it costs much more: the production of large, nutrient-rich eggs and often a huge expenditure of energy and time. In more than 90 percent of mammal species, a male’s only investment in offspring is his sperm, for females provide all the parental care.

This asymmetry between males and females in potential numbers of mates and offspring leads to conflicting interests when it comes time to choose a mate. Males have little to lose by mating with a “substandard” female (say, one who is weak or sickly), because they can easily mate again, and repeatedly. Selection then favors genes that make a male promiscuous, relentlessly trying to mate with nearly any female. (Or any
thing
bearing the slightest resemblance to a female—male sage grouse, for instance, sometimes try to mate with piles of cow manure, and, as we learned earlier, some orchids get pollinated by luring randy male bees to copulate with their petals.)

Females are different. Because of their higher investment in eggs and offspring, their best tactic is to be picky rather than promiscuous. Females must make each opportunity count by choosing the best possible father to fertilize their limited number of eggs. They should therefore inspect potential mates very closely.

What this adds up to is that, in general, males must compete for females. Males should be promiscuous, females coy. The life of a male should be one of internecine conflict, constantly vying with his fellows for mates. The good males, either more attractive or more vigorous, will often secure a large number of mates (they will presumably be preferred by more females too), while substandard males go unmated. Almost all females, on the other hand, will eventually find mates. Since every male is competing for them, their distribution of mating success will be more even.

Biologists describe this difference by saying that the
variance
in mating success should be higher for males than females. Is it? Yes, we often see such a difference. In the red deer, for example, the variation among males in how many offspring they leave during their lifetime is three times higher than that of females. The disparity is even greater for elephant seals, in which fewer than 10 percent of all males leave
any
offspring over several breeding seasons, compared to more than half of the females.
³⁴

The difference between males and females in their potential number of offspring drives the evolution of both male-male competition and female choice. Males must compete to fertilize a limited number of eggs. That’s why we see the “law of battle”: the direct competition between males to leave their genes to the next generation. And that is also why males are colorful, or have displays, mating calls, bowers, and the like, for that is their way of saying “Pick me, pick me!” And it is ultimately female preference that drives the evolution of longer tails, more vigorous displays, and louder songs in males.

Now, the scenario I have just described is a generalization, and there are exceptions. Some species are monogamous, with both males and females providing parental care. Evolution can favor monogamy if males have more offspring by helping with child care than if they abandon their offspring to seek more matings. In many birds, for example, two full-time parents are required: when one goes off to forage, the other incubates the eggs. But monogamous species are not that common in the wild. Only 2 percent of all mammal species, for instance, have this type of mating system.

Further, there are explanations for sexual dimorphism in body size that do not involve sexual selection. In the fruit flies I study, for example, females may be larger simply because they need to produce large and costly eggs. Or males and females might be more efficient predators if they specialize on different food items. Natural selection for reduced competition between members of the two sexes could lead them to evolve differences in body size. This may explain a dimorphism in some lizards and hawks, in which females are larger than males and also catch larger prey.

CURIOUSLY, we also see sexual dimorphisms in many “socially monogamous” species—those in which males and females pair up and rear young together. Since males don’t seem to be competing for females, why have they evolved bright colors and ornaments? This seeming contradiction actually provides further support for sexual selection theory. It turns out that in these cases, appearances are deceiving. The species are socially monogamous but not
actually
monogamous.

One of these species is the splendid fairy wren of Australia, studied by my University of Chicago colleague Stephen Pruett-Jones. At first glance, this species looks like the paragon of monogamy. Males and females usually spend their entire adult lives socially bonded to each other, and they code-fend their territory and share parental care. Yet they show striking sexual dimorphism in plumage: males are a gorgeous iridescent blue and black, while females are a dull grayish brown. Why? Because adultery is rife. When it comes time to mate, females mate with
other
males more often than they do with their “social mate.” (This is shown by DNA paternity analysis.) Males play the same game, actively seeking and soliciting “extra-pair” matings, but they still vary far more than females in their reproductive success. Sexual selection associated with these adulterous couplings almost certainly produced the evolution of color differences between the sexes. This wren is not unique in its behavior. Although 90 percent of all bird species are socially monogamous, in fully three-quarters of these species males and females mate with individuals other than their social partner.

Sexual selection theory makes testable predictions. If only one sex has bright plumage or antlers, performs vigorous mating displays, or builds elaborate structures to lure females, you can bet that it is members of that sex who compete to mate with members of the other. And species showing less sexual dimorphism in behavior or appearance should be more monogamous: if males and females pair up and don’t stray from their mates, there is no sexual competition and therefore no sexual selection. Indeed, biologists see strong correlations between mating systems and sexual dimorphism. Extreme dimorphisms in size, color, or behavior are found in those species, like the birds of paradise or elephant seals, in which males compete for females, and only a few males get most of the matings. Species in which males and females look similar—for instance, geese, penguins, pigeons, and parrots—tend to be truly monogamous, exemplars of animal fidelity. This correlation is another triumph for evolutionary theory, for it is predicted only by the idea of sexual selection and not by any creationist alternative. Why should there be a correlation between color and mating system unless evolution is true? Indeed, it is creationists rather than evolutionists who should become sick at the sight of a peacock’s feather.
³⁵

So far we’ve talked about sexual selection as if the promiscuous sex is always male and the picky sex female. But sometimes, albeit rarely, it’s the other way around. And when these behaviors switch between the sexes, so does the direction of dimorphism. We see this reversal in those most appealing of fish, seahorses, and their close relatives the pipefish. In some of these species the males rather than the females become pregnant! How can that happen? Although the female does produce eggs, after a male fertilizes them he places them in a specialized brood pouch on his belly or tail, and carries them about until they hatch. Males carry only one brood at a time, and their “gestation” period lasts longer than it takes a female to produce a fresh batch of eggs. Males, then, actually invest more in child-rearing than do females. Also, because there are more females carrying unfertilized eggs than males to accept them, females must compete for the rare “nonpregnant” males. Here, the male-female difference in reproductive strategy is reversed. And just as you might expect under sexual-selection theory, it is the females who are decorated with bright colors and body ornaments, while males are relatively drab.

The same goes for the phalaropes, three species of graceful shorebirds that breed in Europe and North America. These are among the few examples of a polyandrous (“one female and many male”) mating system. (This rare mating system can also be found among a few human populations, including Tibetans.) Male phalaropes are entirely responsible for child care, building the nests and feeding the brood while the female moves on to mate with other males. The male’s investment in offspring, then, is greater than the female’s, and females compete for males who will take care of their young. And, sure enough, in all three species females are colored much brighter than males.

Seahorses, pipefish, and phalaropes are the exceptions that prove the rule. Their “reverse” decoration is exactly what one would expect if the evolutionary explanation of sexual dimorphism is true, but doesn’t make sense if these species were specially created.

LET’S RETURN TO “NORMAL” MATE CHOICE, in which females are the choosy ones. What exactly are they looking for when they pick a male? This question inspired a famous disagreement in evolutionary biology. Alfred Russel Wallace, as we’ve seen, was dubious (and ultimately wrong) about whether females are even choosy. His own theory was that females were less colorful than males because they needed to be camouflaged from predators, while the bright colors and ornaments of males were by-products of their physiology. He gave no explanation, though, why males shouldn’t be camouflaged as well.

Darwin’s theory was a little better. He felt strongly that male calls, colors, and ornaments evolved via female choice. On what basis were females choosing? His answer was surprising: pure aesthetics. Darwin saw no reason why females should choose things like elaborate songs or long tails unless they found them intrinsically appealing. His pioneering study of sexual selection,
The Descent of Man, and Selection in Relation to Sex
(1871), is larded with quaint anthropomorphic descriptions of how female animals are “charmed” and “wooed” by various features of males. Yet, as Wallace noted, there was still a problem. Did animals, particularly simple ones like beetles and flies, really have an aesthetic sense like our own? Darwin punted on this one, pleading ignorance:

It turns out that Darwin, though he didn’t have all the answers, was closer to the truth than was Wallace. Yes, females do choose, and that choice seems to explain sexual dimorphisms. But it doesn’t make sense that female preference is based solely on aesthetics. Closely related species, like the New Guinea birds of paradise, have males with very different types of plumage and mating behavior. Is what is beautiful to one species so different from what is beautiful to its closest relatives?

In fact, we now have a lot of evidence that female preferences are themselves adaptive, because preferring certain types of males helps females spread their genes. Preferences aren’t always a matter of random inborn taste, as Darwin supposed, but in many cases probably evolved by selection.