Samoan Butterflies Evolve Rapidly and Avoid Extinction

A male Blue Moon or Great Eggfly butterfly, Hypolimnas bolina.

A butterfly-killing bacteria that is only lethal to males has given rise to skewed sex ratios in populations of this species on two islands in the South Pacific, but researchers have found that male butterflies on one island have bounced back, thanks to the rise of a suppressor gene. [larger].

In a dramatic demonstration of how quickly evolution can occur, a butterfly species that is found on two adjacent islands in the South Pacific Ocean has rapidly evolved genetic defenses against a bacterial parasite that is lethal only to males of the species.

In 2001, an international team of researchers surveyed Blue Moon butterflies (also known as Great Eggfly butterflies), Hypolimnas bolina (pictured above), found on neighboring islands in Samoa and discovered that males were extremely rare, comprising only one percent of the total population. However, when the researchers returned to survey the butterflies again in 2005 and 2006, they found that the sexes had achieved parity (1:1) on one island, and were approaching parity on the other island.

This evolutionary change in the sex ratios of these butterflies took only ten generations to occur.

"To my knowledge, this is the fastest evolutionary change that has ever been observed," said Sylvain Charlat, lead author on the study and a post-doctoral researcher at the University of California, Berkeley.

"We usually think of natural selection as acting slowly, over hundreds of thousands of years," added Gregory Hurst, a senior author on the paper and a researcher in evolutionary genetics at University College London. "But the example in this study happened in the blink of the eye, in terms of evolutionary time, and is a remarkable thing to get to observe."

The parasite that the butterflies are infected with is the bacteria, Wolbachia. This bacteria lives in female Blue Moon butterflies and infects their eggs. Before these infected eggs hatch, the bacteria selectively kill male embryos while remaining alive in the female offspring after they hatch, where the cycle then repeats itself.

When the butterflies were initially surveyed in 2001, the populations showed a 100:1 ratio of females to males on two adjacent islands, Upolu and Savaii. However, when the researchers returned in 2005, they found that the butterflies had reverted to their original sex ratio of 1:1 on Upolu, whereas the population found on Savaii still had a severely skewed sex ratio of 100:1. But by the following year, the team surveyed the Savaii butterflies again and found that nearly all the local populations had achieved sex ratio parity or were nearly at parity, a mere ten generations later.

The team ran genetic analyses and found that the Wolbachia bacteria were still present in butterflies from both islands and it was still capable of killing the male of the species. However, other lab experiments indicated that the males had evolved a special suppressor gene to protect them against the lethal effects of the bacteria, which then allowed their numbers to increase rapidly.

"The suppressor gene allows infected females to produce males," Charlat explained. "These males will mate with many, many females, and the suppressor gene will therefore be in more and more individuals over generations."

The origin of this supressor gene is unknown, but it was not present on either island in 2001, as indicated by the dramatically skewed sex ratio in the butterfly populations. It is not yet clear whether the suppressor gene emerged from a random mutation from within the local population, or if it was introduced by migratory Southeast Asian butterflies in which a supressor gene has already been established.

"But regardless of which of the two sources of the suppressor gene is correct, natural selection is the next step," explained Charlat.

This research shows an interesting pattern of rapid gene flow and geographic spread, and is a nice documentation of rapid natural selection at work.

"This study shows that when a population experiences very intense selective pressures, such as an extremely skewed sex ratio, evolution can happen very fast," observed Charlat.

Also, this research fulfills a prediction made by WD Hamilton in 1967 (Science, 156:477-488). Hamilton predicted that a system where there are gender-ratio disrupters and disrupter suppressor genes could result in dramatic and rapid shifts in gender ratios. I like mentioning this prediction because creationists and other evolution deniers like to (erroneously) claim that biologists never make predictions.

Further, the change in the sex ratio of Blue Moon butterfly populations shows not only that species can evolve very rapidly, but also reveals the importance of parasites as evolutionary drivers, the authors wrote in their paper.

"In the case of H. bolina, we're witnessing an evolutionary arms race between the parasite and the host. This strengthens the view that parasites can be major drivers in evolution," said Charlat.

This study appears in the journal, Science.


Extraordinary Flux in Sex Ratio by Sylvain Charlat, Emily A. Hornett, James H. Fullard, Neil Davies, George K. Roderick, Nina Wedell and Gregory D. D. Hurst Science 317:214 (13 July 2007) [PDF].

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I've steered clear of Wolbachia work. Not because there's anything wrong, but because it always seems so complicated. I reckon I'd have to put some serious effort into working out how the dynamics work. Which is annoying in one sense - it's a fascinating system.