FITNESS FLAW: Reproductively prodigious male and female flies produce less fit offspring of the opposite sex in the lab, implying a genetic tug-of-war between the sexes.
© B. BORRELL CASALS; FRANK LANE PICTURE AGENCY/CORBIS

Sometimes hunting down the best mate can backfire. The theory of sexual selection posits that choosy females seek out mates with elaborate antlers or splashy plumage, for example, because these traits might signify good genes that will lead to hearty offspring. But researchers report that top-breeding fruit flies of both sexes produced worse-breeding descendents, primarily because the mating prowess of each parent did not translate to offspring of the opposite sex. The result supports the idea that some genes can be good for one gender but bad for the other, which may limit the power of sexual selection.

In theory, sexual selection should weed out the less useful genes over time, but animals are nonetheless extremely variable in their genes, notes evolutionary geneticist Adam Chippindale of Queens University in Kingston, Ontario. One reason could be that the same genes are beneficial to one sex but harmful to the other, resulting in a genetic tug-of-war. If true, males or females that have high "fitness" (generate lots of offspring) compared with their counterparts would produce relatively unfit offspring of the other sex. "There could be kind of a dark side to 'good' genes," Chippindale says. Despite some experimental signs of such fitness reversals, researchers had not tested the effect thoroughly in the lab.

To identify a reversal, Chippindale and his colleague Alison Pischedda raised multiple lines of male and female Drosophila melanogaster, some of high fitness and others of low fitness. The researchers then mated the flies in all possible combinations and measured their progeny¿s reproductive success. As predicted, flies that found fit mates got a bum deal: Sons of fit mothers were 11 percent less fit than those of unfit moms, and daughters of fit dads were 7 percent less fit than their counterparts. Fit moms at least made up for some of the deficit with their daughters, which were 7 percent more fit than the rest. Not so for fit dads; the fitness of fathers had no effect on that of sons, presumably because the genes that made the dads fit were on their X chromosomes, which were not passed down to sons, the researchers report in the November issue of PLoS Biology.

"It's an extremely counterintuitive result," says evolutionary biologist Scott Pitnick of Syracuse University. "I actually think this has huge potential for a lot of evolutionary questions, like the maintaining of homosexuality, which really plague evolutionary biology. It's a mechanism for maintaining a tremendous amount of variation." Given that Drosophila is raised in the lab, it's unclear how pervasive the effect might be across species, Chippindale says. "These genes are out there and could be taking the edge off selection," he notes. "It's just a matter of how important they will be in the wild."