The males of many species impress potential mates with brilliant plumage, massive antlers, or expensive cars. Water striders, however, don't go in for courtship. For these smoothly gliding pond insects, mating is a wrestling match in which the male grips the female's head and pins her down while she struggles to throw him off. Now researchers have done a bit of reverse evolution to figure out how males developed this ability in the first place.
Animals that nurture their young together choose mates that will be the best protectors or nest-builders. But as evolutionary biologist Locke Rowe of the University of Toronto in Canada explains, "In some species, males and females have competing interests." Among water striders, for example, neither parent tends the offspring. The female's only job is to produce eggs; the males are mere sperm donors.
Once the female has mated, further couplings with other males are not only unnecessary, but costly. In a typical encounter, the male grabs the female from behind, then both flip over on their backs while the male uses his three pairs of legs to immobilize hers. They then flip back to their original position for copulation, which lasts several minutes. A female hobbled in this way can't catch food, and she's a bigger target for predators while wrestling with another bug. So a female whose eggs have already been fertilized by one male will fiercely reject the advances of other hopeful suitors.
To compete in this battle of the sexes, males in some water strider species have evolved an elaborate set of hooks and spikes on their antennae that precisely conform to the shape of the female's head—helping them maintain their grip long enough to mate. In the new study, Rowe and colleagues have uncovered a gene responsible for this adaptation.
Teasing out the genes that underlie evolutionary change is a challenge, says Rowe. Observing differences among species in the wild doesn't point to the genes involved, while manipulating the genomes of lab workhorses like the fruit fly yields little information about what happens in the natural world.
Rowe and colleagues focused on the water strider Rheumatobates rileyi as a good model for bridging this gap. The researchers took high-speed videos of the insects mating, then used scanning electron microscopes to get detailed pictures of the males' appendages. Finally, they scanned the bugs' genomes to see which genes are active while the antennae develop their elaborate hooks and spines (a process that begins in the larval stages). The search led to one gene, "distal-less," that generates the specialized antennae.
Turning down the function of this gene with a technique called RNA interference (RNAi) resulted in underdeveloped antennae, the team reports online today in Science. The researchers took advantage of the fact that, for reasons that aren't entirely understood, RNAi varies in its effectiveness. The varying degrees of interference resulted in male water striders with a range of antenna styles from completely undeveloped, the way the bugs' ancestors must have looked; through several stages with partly developed hooks; and all the way to the elaborately armed insects of today.
The team then tested the variously equipped water striders with females. As expected, the less developed the males' antennae, the earlier in the mating struggle the females flung them off. Even in normal males studied for comparison, only about 12% of mating attempts led to copulation; the males with undifferentiated antennae had almost no luck.
"Essentially, we turned back time to produce insects at several stages of evolution," says Rowe. He says the study is one of only a handful that connect the dots between the forces of selection (the male versus female struggle), the adaptive change (the antennae), the consequences (success in mating), and the genetic basis.
"It's a fabulous piece of work," says evolutionary biologist Dolph Schluter of the University of British Columbia, Vancouver in Canada. Schluter, who studies the genes that underlie adaptation in stickleback fish, says he is especially impressed with the researchers' molecular surgery. "The approach has enormous potential for studying how natural and sexual selection produce evolutionary novelty."