Why Evolution Is True (26 page)

This is male competition, pure and simple, and the prize is reproduction. It is easy to see how, given this mating system, sexual selection promotes the evolution of large, fierce males: bigger males leave their genes to the next generation, smaller ones don’t. (Females, who don’t have to fight, are presumably close to their optimal weight for reproduction.) Sexual dimorphism of body size in many species—including our own—may be due to competition between males for access to females.

Male birds often compete fiercely over real estate. In many species, males attract females only by controlling a patch of land—one with good vegetation—that is suitable for nesting. Once they have their patch, males defend it with visual and vocal displays, as well as direct attacks on encroaching males. Many of the birdsongs that delight our ears are actually threats, warning other males to keep away.

The red-winged blackbird of North America defends territories in open habitats, usually freshwater marshes. Like elephant seals, this species is polygynous, with some males having as many as fifteen females nesting in their territory. Many other males, called “floaters,” go unmated. Floaters constantly try to invade established territories to sneak copulations with females, keeping resident males busy driving them away. Up to a quarter of a male’s time can be spent vigilantly protecting his turf. Besides direct patrolling, redwing males defend their territories by singing complex songs and making threat displays with their eponymous ornament, a bright red epaulet on the shoulder. (Females are brown, sometimes with a small, vestigial epaulet.) The epaulets aren’t there to attract females—rather, they are used to threaten other males in the battle for territories. When experimenters effaced the epaulets of males by painting them black, 70 percent of males lost their territories, compared to only 10 percent of control males painted with a clear solvent. The epaulets probably keep intruders away by signaling that a territory is occupied. Song is also important. Muted males, temporarily deprived of their ability to sing, also lose territories.

In blackbirds, then, song and plumage help a male get more mates. In the studies described above, and many others as well, researchers have shown that sexual selection is acting because males with more elaborate features get a greater payoff in offspring. This conclusion seems simple but required hundreds of hours of tedious fieldwork by inquisitive biologists. Sequencing DNA in a gleaming lab may seem far more glamorous, but the only way a scientist can tell us how selection acts in nature is to get dirty in the field.

Sexual selection doesn’t end with the sex act itself: males can continue to compete even after mating. In many species, females mate with more than one male over a short period of time. After a male inseminates a female, how can he prevent other males from fertilizing her and stealing his paternity? This
post-mating competition
has produced some of the most intriguing features built by sexual selection. Sometimes a male hangs around after mating, guarding his female against other suitors. When you see a pair of dragonflies attached to each other, it’s likely that the male is simply guarding the female after having fertilized her, physically blocking access by other males. A Central American millipede has taken mate guarding to the extreme: after fertilizing a female, the male simply rides her for several days, preventing any competitor from claiming her eggs. Chemicals can also do this job. The ejaculate of some snakes and rodents contains substances that temporarily plug up a female’s reproductive tract after mating, barricading out other probing males. In the group of fruit flies on which I work, the male injects the female with an antiaphrodisiac, a chemical in his semen that makes her unwilling to remate for several days.

Males use a variety of defensive weapons to guard their paternity. But they can be even more devious—many have
offensive
weapons to get rid of the sperm from previously mating males and replace it with their own. One of the cleverest devices is the “penis scoop” of some damselflies. When a male mates with an already mated female, he uses backward-pointing spines on his penis to scoop out the sperm of earlier-mating males. Only after she’s despermed does he transfer his own sperm. In
Drosophila,
my own lab found that a male’s ejaculate contains substances that inactivate the stored sperm of males who mated previously.

What about the second form of sexual selection: mate choice? Compared to male-male competition, we know a lot less about how this process works. That’s because the significance of colors, plumage, and display is far less obvious than that of antlers and other weapons.

To figure out how mate choice evolves, let’s begin with that pesky peacock tail that caused Darwin such angst. Much of the work on mate choice in the peacock has been done by Marion Petrie and her colleagues, who study a free-ranging population in Whipsnade Park, Bedfordshire, England. In this species males assemble at
leks
, areas where they all display together, giving females an opportunity to compare them directly. Not all males join the lek, but only the ones who do can win a female. One observational study of ten lekking males showed a strong correlation between the number of eyespots in a male’s tail feathers and the number of matings he achieved: the most elaborate male, with 160 eyespots, garnered 36 percent of all copulations.

This suggests that more elaborate tails are preferred by females, but doesn’t prove it. It’s possible that some other aspect of male courtship-say, the vigor of his display—is really what females are choosing, and this just happens to be correlated with plumage. To rule this out, one can do experimental manipulations: change the number of eyespots on the tail of a peacock and see if this affects his ability to get mates. Remarkably, such an experiment was suggested in 1869 by Darwin’s competitor, Alfred Russel Wallace. Although the two men agreed on many things, most notably natural selection, they parted ways when it came to sexual selection. The idea of male-male competition was no problem for either man, but Wallace frowned on the possibility of female choice. Nevertheless, he kept an open mind on this issue, and was way ahead of his time in suggesting how to test it:

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 in 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 yet 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.