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 byproducts 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:
Although we have some positive evidence that birds appreciate bright and beautiful objects, as with the bower-birds of Australia, and although they certainly appreciate the power of song, yet I fully admit that it is astonishing that the females of many birds and some mammals should be endowed with sufficient taste to appreciate ornaments, which we have reason to attribute to sexual selection; and this is even more astonishing in the case of reptiles, fish, and insects. But we really know little about the minds of the lower animals.
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 and inborn taste, as Darwin supposed, but in many cases probably evolved by selection.
What does a female have to gain by choosing a particular male? There are two answers. She can benefit directly, that is, by picking a male who will helps her produce more or healthier young during the act of child care. Or she can benefit indirectly, by choosing a male who has better genes than those of other males (that is, genes that will give her offspring a leg up in the next generation). Either way, the evolution of female preferences will be favored by selection—natural selection.
Take direct benefits. A gene that tells a female to mate with males holding better territories provides her with offspring who are better nourished or occupy better nests. They will survive better and reproduce more than young who were not brought up in good territories. This means that the population of young will contain a higher proportion of females carrying the "preference gene" than it did in the previous generation. As generations pass and evolution continues, every female will eventually carry preference genes. And if there are other mutations that increase the preference for better territories, those too will increase in frequency. Over time, the preference for males with better territories will evolve to be stronger and stronger. And this, in turn, selects on the males to compete more strongly for territories. The female preference evolves hand in hand with the male competition for real estate.
Genes that give indirect benefits to choosy females will also spread. Imagine that a male has genes that make him more resistant than other males to disease. A female who mates with such a male will have offspring that are also more disease-resistant. This gives her an evolutionary benefit to choosing that male. Now imagine as well that there is a gene that enables females to identify these healthier males as mates. If she mates with such a male, that mating will produce sons and daughters who carry both types of genes: those for disease resistance as well as those for preferring males with disease resistance. In each generation, the most disease-resistant individuals, who reproduce better, will also carry genes that tell females to choose the most resistant males. As those resistance genes spread by natural selection, the genes for female preference piggyback along with them. In this way both female preference and disease resistance increase within a species.
Both of these scenarios explain why females prefer certain kinds of males, but not why they prefer certain features of those males, like bright colors or elaborate plumage. This probably happens because those particular features tell the female that a male will provide larger direct or indirect benefits. Let's look at a few examples of female choice.
The house finch of North America is sexually dimorphic for color: females are brown but males have bright colors on their head and breast. Males don't defend territories but do show parental care. Geoff Hill at the University of Michigan found that in one local population, males varied in color from pale yellow through orange to bright red. Wanting to see if color affected reproductive success, he used hair dyes to make males brighter or paler. Sure enough, brighter males obtained significantly more mates than paler ones. And among unmanipulated birds, females deserted the nests of lighter males more often than the nests of brighter males.
Why do female finches prefer brighter males? In the same population, Hill showed that brighter males feed their young more often than do lighter males. Females thus get a direct benefit, in the form of better provisioning of their offspring, by choosing brighter males. (Females mated to lighter males might abandon their nests because the young aren't adequately fed.) And why do brighter males bring more food? Probably because brightness is a sign of overall health. The red color of male finches comes entirely from carotenoid pigments in the seeds they eat—they can't make this pigment on their own. Brighter males are therefore better fed, and probably healthier in general. Females seem to choose bright males simply because the color tells them, "I'm a male who's better able to stock the family larder." Any genes that make females prefer brighter males gives those females a direct benefit, and so selection would increase that preference. And with the preference in place, any male who is better at converting seeds into bright plumage would also get an advantage, because he'll secure more mates. Over time, sexual selection will exaggerate a male's red color. The females stay drab because they gain no benefit from being bright; indeed, they could suffer by becoming more conspicuous to predators.
There are other direct benefits to choosing a healthy and vigorous male. Males can carry parasites or diseases that they can transmit to females, their young, or both, and it's to a female's advantage to avoid these males. A male's color, plumage, and behavior can be a clue to whether he's diseased or infested: only healthy males can sing a loud song, perform a vigorous display, or grow a bright, handsome set of feathers. If males of a species are normally bright blue, for example, you'd best avoid mating with a pale blue male.
Evolutionary theory shows that females should prefer any trait showing that a male will be a good father. All that's required is that there be some genes increasing the preference for that trait, and that variation in the expression of the trait gives a clue to the male's condition. The rest follows automatically. In sage grouse, parasitic lice produce spots of blood on the male's vocal sac, a feature prominently displayed as a swollen, translucent pouch while they're strutting on the lek. Males who have artificial blood spots painted on their vocal sacs get significantly fewer matings: the spots may tip off females that a male is infested and would literally be a lousy father. Selection will favor genes that promote not only the female preference for unspotted sacs, but also the male trait that indicates his condition. The male's vocal sac will get bigger, and the female's preference for the plain vocal sac will increase. This can lead to the evolution of highly exaggerated features in males, like the ludicrously long tail of the widowbird. The whole process stops only when the male trait becomes so exaggerated that any further increase reduces his survival more than it attracts females, so that his net production of offspring suffers.
What about female preferences that give indirect benefits? The most obvious such benefit is what a male always gives to his offspring—his genes. And the same type of traits that show a male is healthy could also show that he's genetically well endowed. Males with brighter colors, longer tails, or louder calls may be able to display these features only if they have genes that make them survive or reproduce better than their competitors. Likewise for males able to build elaborate bowers, or pile up large cairns of stones. You can imagine many features that could show a male has genes for greater survival, or a greater ability to reproduce. Evolutionary theory shows that in these cases, three types of genes will all increase in frequency together: genes for a male "indicator" trait reflecting that he has good genes, genes that make a female prefer that indicator trait, and of course the "good" genes whose presence is reflected by the indicator. This is a complex scenario, but most evolutionary biologists consider it the best explanation for elaborate male traits and behaviors.
But how can we test whether the "good genes" model is really correct? Are females looking for direct or indirect benefits? A female might spurn a less vigorous or less showy male, but this might reflect not his poor genetic endowment but simply an environmentally caused debility, such as infection or malnutrition. Such complications make the causes of sexual selection in any given case hard to unravel.
Perhaps the best test of the good-genes model was done on gray tree frogs by Allison Welch and her colleagues at the University of Missouri.
Male frogs attract females by giving loud calls, limning summer nights in the southern United States. Studies of captive frogs show that females strongly prefer males whose calls are longer. To test whether those males had better genes, researchers stripped eggs from different females, fertilizing half of each female's eggs in vitro with sperm from long-calling males, and the other half with sperm from short-calling males. The tadpoles from these crosses were then reared to maturity. The results were dramatic. Offspring from long-callers grew faster and survived better as tadpoles, were larger at metamorphosis (the time when tadpoles turn into frogs), and grew faster after metamorphosis. Since male gray tree frogs make no contribution to offspring except for sperm, females can get no direct benefits from choosing a long-calling male. This test strongly suggests that a long call is the sign of a healthy male with good genes, and that females who choose those males produce genetically superior offspring.
So what about those peacocks? We've seen that females prefer to mate with males who have more eyespots in their tails. And males make no contribution to raising their young. Working at Whipsnade Park, Marion Petrie showed that males with more eyespots produce young that not only grow faster but also survive better. It's likely that by choosing more elaborate tails, females are choosing good genes, for a genetically well-endowed male is more capable of growing an elaborate tail.
These two studies are all the evidence we have so far that females choose males with better genes. And a fair number of studies have found no association between mate preference and the genetic quality of offspring. Still, the good-genes model remains the favored explanation of sexual selection. This belief, in the face of relatively sparse evidence, may partly reflect a preference of evolutionists for strict Darwinian explanations—a belief that females must somehow be able to discriminate among the genes of males.
There is, however, a third explanation for sexual dimorphisms, and it's the simplest of all. It is based on what are called sensory-bias models. These models assume that the evolution of sexual dimorphisms is driven simply by preexisting biases in a female's nervous system. And those biases could be a by-product of natural selection for some function other than finding mates, like finding food. Suppose, for example, that members of a species had evolved a visual preference for red color because that preference helped them locate ripe fruits and berries. If a mutant male appeared with a patch of red on his breast, he might be preferred by females simply because of this preexisting preference. Red males would then have an advantage, and a color dimorphism could evolve. (We assume that red color is disadvantageous in females because it attracts predators.) Alternatively, females may also simply like novel features that somehow stimulate their nervous systems. They may, for example prefer bigger males, males who hold their interest by doing more complex displays, or males who are shaped oddly because they have longer tails. Unlike the models I described earlier, in the sensory-bias model females derive neither direct nor indirect benefits from choosing a particular male.
You could test this theory by producing a truly novel trait in males and seeing if females like it. This was done in two species of Australian grassfinches by Nancy Burley and Richard Symanski at the University of California. They simply glued a single vertically pointing feather to the heads of males, forming an artificial crest, and then exposed these crested males, along with uncrested controls, to females. (Grassfinches don't have head crests, although some unrelated species, like cockatoos, do.) Females turned out to show a very strong preference for males sporting white artificial crests over males with either red or green crests, or normal uncrested males. We don't understand why females prefer white, but it may be because they line their nests with white feathers to camouflage their eggs from predators. Similar experiments in frogs and fish also show that females have preferences for traits to which they've never been exposed.36 The sensory-bias model maybe important, since natural selection may often create pre-existing preferences that help animals survive and reproduce, and these preferences can be co-opted by sexual selection to create new male traits. Maybe Darwin's theory of animal aesthetics was partly correct, even if he did anthropomorphize female preferences as a "taste for the beautiful."
Conspicuously missing from this chapter has been any discussion of our own species. What about us? How far theories of sexual selection apply to humans is a complicated question—one that we'll pursue in chapter 9.
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