Butterflies evolve resistance to male-killing bacteria in record time

This is the third of eight posts on evolutionary research to celebrate Darwin’s bicentennial.

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In our world, there is (roughly) one man for every woman. Despite various social differences, our gender ratio remains steadfastly equal, so much so that we tend to take it for granted. Elsewhere in the nature, things are not quite so balanced.

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Take the blue moon butterfly (Hypolimnas bolina). In 2001, Emily Dyson and Greg Hurst were studying this stunningly beautiful insect on the Samoan islands of Savaii and Upolu when they noticed something strange – almost all the butterflies were females. In fact, the vastly outnumbered males only made up 1% of the population.

The cause of this female-dominated world was an infection, an inherited bacterium called Wolbachia. Wolbachia is a strong candidate for the planet’s most successful parasite for it infects a huge proportions of the world’s arthropods, themselves a highly successful group. And it does not like males.

Wolbachia has an easy route of infection – it can be passed to the next generation through the eggs of an infected female. But it can’t get into sperm, and for that reason, male insects are useless to it and it has a number of strategies for dealing with them. Sometimes it allows females to reproduce without male fertilisation. At other times, it forces males to undergo sex changes to become females. But in cases like the blue moon butterfly, it simply kills the males outright before they’ve even hatched from their eggs.

In 2001, Dyson and Hurst noted that the islands with the fewest males were the ones with the most prevalent Wolbachia infections. But by 2005, things had changed. Sylvain Charlat from University College London, along with Hurst and others, found that males were increasing in number all around Upolu Island. A year later, a formal survey confirmed the males’ amazing comeback.

On Upolu, they equalled the females in number. Within just 10 generations, the male butterflies had gone from being outnumbered a hundred to one to an equal footing with the females. “To my knowledge, this is the fastest evolutionary change that has ever been observed,” said Charlat. In just ten generations, they evolved resistance to the parasite – a dramatic example of natural selection in action.

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Charlat found the same story at a site on Savaii Island close to neighbouring Upolu. On the other side of the island, the males were still in the minority and many failed to hatch. But at 7% of the population, they were doing better than they had done in five years before.

All the butterflies were still infected with the same Wolbachia strain that had slaughtered their males just a few years back. And the bacteria themselves had not changed – when Charlat mated infected females with uninfected males from a different island, the parasite’s male-killing nature resurfaced within a few generations.

Charlat believes that the Upolu butterflies had gained a resistance gene (or several) that allowed them to shrug off the male-killing bacteria. It either evolves the trait itself, or gained it from South-east Asian populations that had already become resistant.

Whatever the origin, the mutation spread like genetic wildfire across the Upolu and onto neighbouring Savaii. Most mutations carry small benefits and spread slowly. But by levelling a populations sex ratio, a mutation that resists Wolbachia clearly provides a huge advantage.

Surviving males who carry the gene(s) would have had their pick of females, since most of their competition lay dead in their eggs. And females that picked up the mutation would have had twice the number of surviving young.

Charlat’s work highlights just how powerful an influence parasites have on the course of evolution. Just how powerful parasites can be in the course of evolution. Events like this may be very commonplace, but at such speed, they may have happened before researchers could spot them.

The butterflies’ newfound resistance is also marvellous example of the Red Queen hypothesis, where parasites and hosts are caught in an evolutionary arms race. Each is forced to acquire new adaptations and counter-adaptations just to stay in the same place.

In this particular arms race, the butterflies have won the battle against Wolbachia. But the war isn’t over. The parasite now faces renewed pressures to find innovative ways of doing away with the dead-end males. How long will it be before it evolves a retaliatory strike?

Reference: Charlat, Hornett, Fullard, Davies, Roderick, Wedell & Hurst. 2007. Extraordinary flux in sex ratio. Science 317: 214.

Images: by JM Garg 

More on Wolbachia and evolutionary arms races:

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