Before Darwin, sexual dimorphism was a mystery. Creationists then— as now—could not explain why a supernatural designer should produce features in one sex, and only one sex, that harms its survival. As the great explainer of nature's diversity, Darwin was naturally anxious to understand how these seemingly pointless traits evolved. He finally noticed the key to their explanation: if traits differ between males and females of a species, the elaborate behaviors, structures, and ornaments are nearly always restricted to males.
By now you might have guessed how these costly traits evolved. Remember that the currency of selection is not really survival, but successful reproduction. Having a fancy tail or a seductive song doesn't help you survive, but may increase your chances of having offspring— and that's how these flamboyant traits and behaviors arose. Darwin was the first to recognize this trade-off, and coined the name for the type of selection responsible for sexually dimorphic features: sexual selection. Sexual selection is simply selection that increases an individual's chance of getting a mate. It's really just a subset of natural selection, but one that deserves its own chapter because of the unique way it operates and the seemingly nonadaptive adaptations it produces.
Sexually selected traits evolve if they more than offset the male's diminished survival with an increase in his reproduction. Maybe wid-owbirds with longer tails don't evade predators very well, but females might prefer the longer-tailed males as mates. Deer with bigger antlers might struggle to survive under a metabolic burden, but perhaps they win jousting contests more frequently, thereby siring more offspring.
Sexual selection comes in two forms. One, exemplified by the Irish elk's huge antlers, is direct competition between males for access to females. The other, the one that produces the widowbird's long tail, is female choosiness among possible mates. Male-male competition (or, in Darwin's oft-pugnacious terminology, "the Law of Battle") is the easiest to understand. As Darwin noted, "It is certain that with almost all animals there is a struggle between the males for the possession of the female." When males of a species battle it out directly, be it through the clashing antlers of deer, the stabbing horns of the stag beetle, the head butting of stalk-eyed flies, or the bloody battles of massive elephant seals, they win access to females by driving off competitors. Selection will favor any trait that promotes such victories so long as the increased chance of getting mates more than offsets any reduced survival. This kind of selection produces armaments: stronger weapons, larger body size, or anything that helps a male win physical contests.
In contrast, features such as bright colors, ornaments, bowers, and mating displays are molded by the second type of sexual selection, mate choice. To female eyes, it seems, not all males are the same. They find some male traits and behaviors more attractive than others, so genes that produce those features accumulate in populations. There is also an element of competition between males in this scenario, but it is indirect: winning males have the loudest voices, the brightest colors, the most alluring pheromones, the sexiest displays, and so on. But in contrast to male-male competition, here the winner is decided by the females.
In both types of sexual selection, males compete for females. Why isn't it the other way around? We'll learn shortly that it all rests on the difference in size between two tiny cells: the sperm and the egg.
Is it really true, though, that males who win contests, or are more highly ornamented, or perform the best displays, actually get more mates? If they don't, the whole theory of sexual selection collapses.
In fact, the evidence strongly and consistently supports the theory. Let's start with contests. The northern elephant seal of North America's Pacific coast shows extreme sexual dimorphism for size. Females are roughly 10 feet long and weigh about 1,500 pounds, while males are nearly twice as long and can weigh up to 6,000 pounds—bigger than a Volkswagen and more than twice as heavy. They are also polygynous: that is, males mate with more than one female during the breeding season. About a third of the males guard harems of females with whom they couple (up to 100 mates for an alpha male!), while the rest of the males are doomed to bachelorhood. Who wins and who loses the mating lottery is determined by fierce contests between males before the females even haul out on the beach. These contests get bloody, with the big bulls bashing their massive bodies together, inflicting deep neck wounds with their teeth and setting up a dominance hierarchy that has the largest males at the top. When the females do arrive, the dominant males herd them into their harems and drive off approaching rivals. In a given year, most pups are sired by just a few of the largest males.
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 bird songs 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 postmating 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 anti-aphrodisiac, 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:
The part that remains to be played by ornament alone will be very small, even if it were proved, which it is not, that a slight superiority in ornament alone usually determines the choice of a mate.
This, however, is a matter that admits of experiment, and I would suggest that either some Zoological Society or any person having the means, should try such experiments. A dozen male birds of the same age—domestic fowls, common pheasants, or gold pheasants, for instance—should be chosen, all known to be acceptable to the hen birds. Half of these should have one or two tail plumes cut off, or the neck plumes a little shortened, just enough to produce such a difference as occurs by variation in nature, but not enough to disfigure the bird, and then observe whether the hens take any notice of the deficiency, and whether they uniformly reject the less ornamented males. Such experiments, carefully made and judiciously varied for a few seasons, would give most valuable information on this interesting question.
In fact, such experiments weren't done until more than a century later. But the results are now in, and female choice is common. In one experiment, Marion Petrie and Tim Halliday cut twenty eyespots off the tail of every male in a group of peacocks, and compared their mating success to that of a control group that was handled but not clipped. Sure enough, in the next breeding season the deornamented males each averaged 2.5 fewer matings than control males.
This experiment certainly suggests that females prefer males whose ornaments had not been reduced. But ideally, we'd also like to do the experiment in the other direction: make the tails more elaborate and see if that enhances mating success. While this is hard to do in peacocks, it's been done in the territorial African long-tailed widowbird by the Swedish biologist Malte Andersson. In this sexually dimorphic species, males have tails about 20 inches long, females about 3 inches. By removing parts of the long male tails and gluing some of these removed parts onto normal tails, Andersson created males with abnormally short tails (6 inches), normal "control" tails (a piece cut off and then glued back on), and long tails (30 inches). As expected, short-tailed males acquired fewer females nesting on their territory compared to normal males. But males with the artificially long tails gained a whopping increase in mat-ings, attracting nearly twice as many females as did normal males.
This raises a question. If males with 30-inch tails won more females, why haven't widowbirds evolved tails that long in the first place? We don't know the answer, but it's likely that having tails that long would reduce a male's longevity more than they would increase his ability to get mates. Twenty inches is probably the length at which total reproductive output, averaged over a lifetime, is near its maximum.
And what do those male sage grouse gain from their arduous antics on the prairie? Again, the answer is mates. Like peacocks, male sage grouse form leks where they display en masse to inspecting females. It's been shown that only the most vigorous males—who "strut" about 800 times per day—win females, while the vast majority of males go unmated.
Sexual selection also explains the architectural feats of bowerbirds. Several studies have shown that the types of bower decorations, which differ in each species, are correlated with mating success. Satin bower-birds, for example, get more mates if they put more blue feathers in their bowers. In spotted bowerbirds, the most success is achieved by displaying green Solanum berries (a species related to wild tomatoes). Joah Madden from Cambridge University stripped the decorations from spotted bowerbird bowers, and then offered the males a choice of sixty objects. Sure enough, they redecorated their bowers mainly with Solanum berries, placing them in the most conspicuous positions on the bower.
I've concentrated on birds because biologists have found it easiest to study mate choice in that group—birds are active during the day and easy to observe—but there are many examples of mate choice in other animals. Female tungara frogs prefer to mate with males who bellow the most complex calls. Female guppies like males with longer tails and more colored spots. Female spiders and fish often prefer larger males. In his exhaustive book Sexual Selection, Malte Andersson describes 232 experiments in 186 species showing that a huge variety of male traits are correlated with mating success, and the vast majority of these tests involve female choice. There is simply no doubt that female choice has driven the evolution of many sexual dimorphisms. Darwin was right after all.
So far we've neglected two important questions: why do females get to do the choosing while males must woo or fight for them? And, why do females choose at all? To answer these questions we must first understand why organisms bother to have sex.
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