Just as parasites might create the rooster’s comb, they might draw out the long tail feathers on birds of paradise. They might make redwing blackbirds redder, they might put bright spots on male stickleback fish, and they might make the sperm packages of crickets bigger. Anything that females could use to judge males might be influenced by parasites.
Hamilton and Zuk presented their idea in the early 1980s, with a simple test. You’d expect that on the whole, the members of a species saddled by many parasites would be showier than a species with a lighter load. According to their hypothesis, bacteria and viruses wouldn’t have a big impact on male display. They tend to kill their hosts or get killed by them. In the first case, there’s no male left to do the displaying; in the second, a sick male could recover so well he’d be indistinguishable from stronger males.
Hamilton and Zuk gathered reports on North American songbirds and their parasites that cause chronic, grinding diseases—bird malaria, for example, and Toxoplasma, trypanosomes, and various worms and flukes. They then rated the showiness of the males of each species in terms of their brightness and their song, and found that the species with the most parasites had the strongest male displays.
That initial work inspired a huge amount of research (more, actually, than Hamilton’s broader theory on the origin of sex itself). Zoologists tested these ideas in the songs of crickets, in the spots on stickleback fish, in the throat pouches of fence lizards. In many of the tests—especially the lab experiments—Hamilton and Zuk fared well. Zuk studied red jungle fowl from Southeast Asia, for example, which are wild relatives of chickens. She kept track of the choices made by female jungle fowl in her lab and measured the combs on the males they chose. Females, she found, consistently preferred males with longer combs.
In a more elaborate study, Swedish scientists studied wild ring-necked pheasants. Male pheasants have spurs on their legs, and the researchers found that the females used the length of the spur to decide which male to mate with. The researchers then looked at the immune system genes of the pheasants and found that the pheasants with the longest spurs shared a particular combination of genes. They don’t know what those genes actually do to help the males fight off parasites. But they observed the offspring of the pheasants and found that the ones with long-spurred fathers had better chances of surviving than those with short-spurred ones.
There’s no reason why these antiparasite advertisements can’t extend beyond a male’s body to the way he courts females. That certainly seems to be what’s going on with the fish Copadichromis eucinostomus, which lives in Lake Malawi in central Africa. To attract females, the males build bowers out of sand on the lake bottom. Some of them are nothing more than a handful of grains sitting on top of boulders, while others are big cones several inches high. The males build their bowers together, creating dense neighborhoods, and each defends his own against roaming males that are trying to usurp him. The female fish spend most of their time feeding on their own, but when the time comes to mate, they go to the bower neighborhood and inspect the males’ work. If a female chooses to mate with a male, she releases an egg and puts it in her mouth. The male puts his sperm in her mouth and she carries away the fertilized egg.
The females apparently use the bowers to find out which males do the best job of fighting parasites such as tapeworms. Experiments have shown that the females prefer males who built big, smoothly shaped bowers, and these males also happen to be the ones who carry the fewest tapeworms. A fish that’s carrying tapeworms may have to spend so much time eating that it can’t maintain its bower. The bower thus becomes a medical chart, and perhaps a genetic profile.
But the Hamilton-Zuk hypothesis has failed several tests as well. Male desert toads attract their mates with their calls, for example, but a loud call doesn’t reflect an immune system better able to fight off Pseudodiplorchis, the parasite that lives in their bladder and drinks their blood. In some species of fence lizards, the males have brightly colored throat flaps that females just adore, but there’s no connection between their brightness and parasites such as Plasmodium that attack the lizards.
These failures have made scientists wonder whether they’ve been testing the Hamilton-Zuk hypothesis the wrong way. A particular parasite may be harmful or harmless, and may therefore have a big influence on a male’s display or none at all. If you have a lot of studies on the loads of different parasites, it’s hard to use them to come up with any sort of general conclusion. Rather than counting the parasites themselves, measuring the immune system may be more reliable. Immune systems have evolved to cope with many different kinds of parasites, so they can offer a better overall clue. It’s a lot harder to count microscopic white blood cells than giant tapeworms, but it turns out to be a better method. Immune studies give the Hamilton-Zuk hypothesis strong, consistent support. Peahens, for example, choose peacocks with more extravagant tails, and researchers have found that peacocks with more extravagant tails have immune systems that can mount a stronger response to parasites.
Another reason why the Hamilton-Zuk hypothesis is falling short may be that scientists are looking at the wrong signals. They’ve stuck with visible cues like rooster combs and lizard pouches because they’re easy to measure. But among the channels of communication between the sexes, vision may not be all that important. Mice, for example, can smell the urine of a prospective mate and tell whether or not it’s carrying parasites; if a male mouse is sick, a female will stay away. It’s even possible that males could use their odors to advertise their strength against parasites with some kind of extravagant, irresistible perfume. “The scent of a male mouse,” writes one biologist, “is the chemical equivalent of a peacock’s plumage.”
And even if Hamilton and Zuk’s idea turns out to fail for other animals, parasites may well have shaped their sex lives anyway for very different reasons. Once again, it all comes down to how a given animal passes on its genes. Among bees, young queens leave their birthplace hive at the end of the summer with a retinue of males. After she mates with them, the males then die, but the queen survives the winter and emerges in the spring to start a new colony with the eggs that were fertilized the previous fall. Every species of bees, in other words, flows through the bottleneck of its few queens.
By studying the DNA of bees, biologists have found that the queens may mate with ten or twenty males during their nuptial flight. That much sex, pleasure aside, is costly: a mating queen is more vulnerable to a predator’s attack, and she could save the energy involved in all that sex to survive the winter.
Bees may be having all that sex as a defense against parasites, as demonstrated by Paul Schmid-Hempel, a Swiss biologist. He injected sperm into queens and then raised the colonies the queens gave birth to. Some queens got the sperm of only a few closely related males, while others got a cocktail with four times more genetic diversity. When the queen’s colony began to hatch, Schmid-Hempel put the colonies out in a flowering meadow near Basel and left them there until the end of the season, when he went out to capture them.
By just about every measure, the offspring of high-diversity queens were far stronger against parasites than were the low-diversity ones. Their colonies had many fewer infections, fewer kinds of parasites invading, and fewer parasites in a given individual. The offspring of high-diversity queens were more likely to survive till the end of the summer, which made it more likely that they’d produce future colonies. Instead of carefully eyeing up a single male to mate, a queen bee may look for many suitors to create a genetic rainbow in her future hive.