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But Madame Butterfly, Where Are All the Males?

Darwin's Rx: natural selection defeats a male-killing bacterial strain and restores a more balanced sex ratio among Samoan blue moon butterflies



SYLVAIN CHARLAT

In one of the swiftest examples of evolutionary adaptation ever observed, scientists have discovered that male blue moon butterflies (Hypolimnas bolina) on the Samoan island of Savaii developed resistance to the selectively male-killing bacteria Wolbachia within 10 generations that spanned less than a year.

An international team of researchers reports in Science today that they found that the number of male butterflies on Savaii jumped from 1 to 39 percent of the island's butterfly population between 2005 and 2006, thanks to this rapid-fire adaptation.

Wolbachia is one of many bacteria that infect arthropods such as butterflies and selectively kill only one sex; its effect on the other sex is benign. By destroying nearly all of an infected female's male embryos, this selective behavior guarantees that all females—almost the entire population—are infected, thereby maximizing the bacteria's spread. Some insects like ladybugs make the best of this predicament, for example, by bearing cannibalistic larvae; the females of the brood increase their food supply by eating their dead male siblings. It is not clear whether the blue moon butterfly also utilizes a Wolbachia infection in some way, but "the females appear to grow better when they're infected," says team member biologist Sylvain Charlat of University College London.

After years of skewed sex ratio, sometime in 2005 a suppressor gene was introduced by an as yet unknown mechanism into female blue moons on Savaii, which made their male offspring resistant to Wolbachia. In a stunning demonstration of the survival of the fittest, the few resistant males mated far and wide, and because the suppressor gene was a dominant trait, resistant males proliferated.

From being almost all-female, the larval population went on to become an equal mix of the sexes in less than a year. Data from two studies in 2001 and 2005 on Upolu, another Samoan island, showed a similar shift in the sex ratio during the intervening four years, but no one caught it in action because it occurred so quickly. Indeed, the study concludes that such fast evolutionary responses to extreme population pressures are probably fairly routine in nature, given that Wolbachia is just one of many sex ratio distorters.

But butterflies are not the only organisms capable of rapid evolution. Is it possible that Wolbachia can in turn evolve to become resistant to the suppressor gene, much like pathogens that develop drug-resistance in humans? "We predict that genetic variations may be present in the bacterial side also, which would restore their male-killing capacity and keep the arms race going," Charlat says. The team is currently trying to answer this and other questions, which include finding the origin of the suppressor mutation.

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