Infected butterflies reverse sex roles

Among butterflies afflicted by bacteria that wipe out most of the guys, females buck a basic trend and become the gender that gathers in frantic swarms to mate, report British researchers.

In most species, it’s the males that crowd into clusters, or leks, to show off for choosy mates, explains Francis M. Jiggins of the University of Cambridge in England. Yet among some of the sub-Saharan butterflies Acraea encedon and Acraea encedana, females gather in odd bunches.

Jiggins linked the roiling clouds of up to 350 female butterflies to a high prevalence of infection with Wolbachia bacteria, which destroy eggs that would have hatched into males. In butterfly haunts with lower infection rates and more-balanced sex ratios, females don’t bother swarming, Jiggins found.

In the Jan. 7 Proceedings of the Royal Society of London B, he and his colleagues argue that a lopsided sex ratio creates a phenomenon practically unknown among animals, a female lek.

“This is the first time people have shown that Wolbachia has changed the mating behavior of its host,” Jiggins notes.

Wolbachia infect an estimated 20 percent of arthropod species. The bacteria spread via eggs of an infected mother and play havoc with reproduction, causing such oddities as virgin births in wasps, mating incompatibilities in mosquitoes, and genetic males with female bodies in wood lice (SN: 11/16/96, p. 318:

In extremely infected populations of the Acraea species that Jiggins studied, less than 10 percent of males survive. The researchers checked butterfly sex ratios, infection rates, and mating behavior at 15 sites in Uganda. In 11 high-infection zones, Jiggins saw females cluster at grassy spots near trees but with no apparent food plant or other resource. At one site, he found that females stopped swarming when the infection rate dropped but started again when the rate rose.

Jiggins wonders whether male butterflies visiting leks get choosy, perhaps selecting uninfected females. However, a male doesn’t seem to spend much time picking a partner. “They appear to collide in midair and tumble to the ground—and mate,” he notes.

“This is an unusual Wolbachia system,” comments John H. Werren of the University of Rochester (N.Y.). The bacterium usually doesn’t kill males.

He predicts that any time an organism gets transmitted only from mother to offspring, killing of males can evolve. Yet the many other male-killing microbes that have been studied only infect 5 to 10 percent of the population, he says.

The notion of any female lek seems “very surprising but not impossible,” says George F. Turner of the University of Southampton in England. Definitions vary, but Jiggins claims at least one precedent for a ladies’ lek. Clouds of female dance flies wait for a male to offer one of them a dead insect as a nuptial gift.

Male leks have raised theoretical puzzles, Turner says. Typically in species with leks, females mate with a male only if it’s “surrounded by a lot of other males fighting and interfering,” he says. “It seems a stupid thing for a female to do.”

Also, he notes a paradox: Males in leks differ from each other even after generations of females choose the same traits. He’d welcome a female lek. He says, “It might give us some insight.”

Susan Milius is the life sciences writer, covering organismal biology and evolution, and has a special passion for plants, fungi and invertebrates. She studied biology and English literature.

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