The drawers of the world’s museums are full of pinned, preserved and catalogued insects. These collections are more than just graveyards – they are a record of evolutionary battles waged between animals and their parasites. Today, these long-dead specimens act as “silent witnesses of evolutionary change”, willing to tell their story to any biologist who knows the right question to ask.
This time round, the biologist was Emily Hornett, currently at UCL, and her question was “How have the ratios of male butterflies to female ones changed over time?” You would think that the sex ratios of insects to mirror the one-to-one proportions expected of humans but not if parasites get involved.
The bacterium Wolbachia is arguably the world’s most successful parasite, infecting around 20% of all insects, themselves an extraordinarily successful group. It can infect eggs but not sperm, which means that females can pass the bacteria on to their offspring, but males cannot. As a result, Wolbachia has it in for males – they are evolutionary dead-ends, and the bacterium has many strategies for getting rid of them. It can kill them outright, it can turn them into females and it can prevent them from mating with uninfected females. As a result, populations infected with Wolbachia can be virtually male-free.
To study the effect of Wolbachia on butterfly populations, Hornett (great name for an entomologist)turned to collections of the blue moon butterfly (Hypolimnas bolina). This beautiful species was heavily collected by entomologists between 1870 and 1930 and their efforts have stocked the museums of the world with specimens. While these were long dead, Hornett found that many of them contained viable DNA and she used them to develop a genetic test for Wolbachia infections.
She validated her Wolbachia test by using butterflies collected by the entomologist H.W.Simmons in Fiji over 70 years ago. Simmons carefully recorded the numbers of males and females in his butterflies and noted some very unusual all-female brood. Sure enough, Hornett confirmed that only mothers who tested positive for Wolbachia produced these skewed clutches, while those that were infection-free gave birth to the standard bisexual broods.
Satisfied that her test was accurate, Hornett cast her net further. She looked at specimens collected from five populations of blue moon butterflies collected from the Phillippines, Borneo, Tahiti, Fiji and Samoa between 73 and 123 years ago. The butterflies are well studied to this day, so Hornett could compare the proportion of Wolbachia infections then and now. In butterfly time, this represents a gap of 500 to 1000 generations separating the specimens from their modern descendants.
The results show that the butterfly and the bacterium have been engaging in a heated evolutionary battle throughout the Pacific. The male-killer’s dominance has fluctuated greatly, rising in some areas and falling in others, while the butterfly has repeatedly evolved to resist its sex-skewing antics.
This is the third of eight posts on evolutionary research to celebrate Darwin’s bicentennial.
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.
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.