Why sex evolved is in fact one of evolution's greatest mysteries. Any individual who reproduces sexually—that is, by making eggs or sperm that contain only half of its genes—sacrifices 50 percent of its genetic contribution to the next generation compared to an individual who reproduces asexually. Let's look at it this way. Suppose that there was a gene in humans whose normal form led to sexual reproduction but whose mutant form enabled a female to reproduce parthenogenetically— by producing eggs that develop without fertilization. (Some animals really do reproduce this way: it's been seen in aphids, fish, and lizards.) The first mutant woman would have only daughters, who themselves would produce more daughters. In contrast, nonmutant, sexually reproducing women would have to mate with males, producing half sons and half daughters. The proportion of women in the population would quickly begin to rise above 50 percent as the pool of females became increasingly full of mutants who produce only daughters. In the end, all the females would be produced by asexually reproducing mothers. Males would become superfluous and disappear: no mutant females would need to mate with them, and all females would give birth to only more females. The gene for parthenogenesis would have outcompeted the gene for sexual reproduction. You can show theoretically that each generation the "asexual" gene would produce twice as many copies of itself as did the original "sexual" gene. Biologists call this situation the "twofold cost of sex." The bottom line is that under natural selection genes for parthenogenesis spread quickly, eliminating sexual reproduction.
But this hasn't happened. The vast majority of Earth's species reproduce sexually, and that form of reproduction has been around for over a billion years.33 Why hasn't the cost of sex led to its replacement by parthenogenesis? Clearly, sex must have some huge evolutionary advantage that outweighs its cost. Although we haven't figured out exactly what that advantage is, there's no shortage of theories. The key may well lie in the random shuffling of genes that occurs during sexual reproduction, which produces new combinations of genes in the offspring. By bringing together several favorable genes in one individual, sex might promote faster evolution to deal with aspects of the environment that are constantly changing—like the parasites that relentlessly evolve to counter our own evolving defenses. Or perhaps sex could purge bad genes from a species by recombining them together into one severely disadvantaged individual, a genetic scapegoat. Yet biologists still question whether any known advantage outweighs the twofold cost of sex.
Once sex has evolved, however, sexual selection follows inevitably if we can explain just two more things. First, why are there just two (rather than three or more) sexes that must mate and combine their genes to produce offspring? And second, why do the two sexes have different numbers and sizes of gametes (males produce a lot of small sperm, females fewer but larger eggs)? The question of the number of sexes is a messy theoretical issue that needn't detain us, except to note that theory shows that two sexes will evolutionarily replace mating systems involving three or more sexes; two sexes is the most robust and stable strategy.
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 pretty 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 females 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'd probably 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.
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