Evolving defenses rapidly suppress male killers



A male nymphalid tropical butterfly Hypolimnas bolina, otherwise known as the Common Eggfly.
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In the game of survival, anything goes--even the selective extermination of males. Male killing is the preferred strategy for a diverse group of bacteria that infect insects and other arthropods. Aside from its tabloid appeal, male killing offers biologists a platform for investigating genetic conflict--evolutionary battles between competing elements within the same genome. Male-killing bacteria are passed from mother to offspring, but only males die from infection, suggesting that males harbor genetic elements that allow them to succumb to infection. In keeping with evolutionary theory, these selfish genetic elements, which spread at the expense of the organism, should engender counteracting elements that promote male survival, but until now scant evidence has linked the evolution of host suppressors to selfish elements that mediate male killing. However, in PLoS Biology today, Emily Hornett, Greg Hurst, and colleagues report the first case of total suppression of male killing in a butterfly, Hypolimnas bolina, infected with the wBol1 strain of the male-killing bacterium Wolbachia.

H. bolina is found throughout the Indo-Pacific. Because wBol1 infection kills males in Polynesia but not in Southeast Asia, breeding individuals from each region could reveal genetic elements in the different populations that favor life over death. And because infected females transmit infection directly to offspring, breeding could also introduce wBol1 genes (and infection) onto the butterfly genetic background (a technique called introgression). The authors therefore carried out breeding experiments to test whether male-killing wBol1 taken from Moorea in Polynesia lose that ability against Southeast Asian males with a Thai or Philippine genetic background, and whether benign wBol1 from Thailand or the Philippines turn lethal against males with a Moorean genetic background. They mated infected Moorean females with Thai and Philippine males, and mated infected Thai and Philippine females with Moorean males. Crossing the Moorean and Southeast Asian populations suppressed the male-killing effects of wBol1 from Moorea in just a single generation--in stark contrast to the control crosses (Moorean females mated with Moorean males), which yielded no males at all. But when Moorean wBol1 infection was reintroduced to its native host background--by backcrossing first-generation hybrid Moorean/Southeast Asian females with wild Moorean males--it became male-lethal again.

The researchers concluded that suppression occurs in the embryo, because male offspring of Moorean females crossed with the Southeast Asian males survived even though the mother's genetic profile allows killing. The fact that first-generation hybrids survived at nearly the same ratio as seen in wild Southeast Asian males, they explain, suggests the effect is dominant (requires just one copy of the gene) and is at high frequency in the population. A dominant effect also explains why male killing didn't occur in first-generation crosses between Southeast Asian females and Moorean males--the suppressor elements had not been segregated out of the population yet. Through simulations, the researchers show that the suppressor could spread through the population in just 100 generations, suggesting that male killing could disappear relatively quickly after a suppressor mutation occurs. Thus, genetic conflict between killing abettors and suppressors may be far more widespread than once thought, but has simply eluded detection. Given the diversity of species afflicted by male-killing bacteria, researchers will have plenty of options for testing this possibility.

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Citation: Hornett EA, Charlat S, Duplouy AMR, Davies N, Roderick GK, et al. (2006) Evolution of male-killer suppression in a natural population. PLoS Biol 4(9): e283. DOI: 10.1371/journal.pbio.0040283.

CONTACT:
Emily Hornett
University College London
4 Stephenson Way
London, NW1 2HE, United Kingdom
+44(0)20-7679-5116
+44(0)20-7679-5052 (fax)
e.hornett@ucl.ac.uk

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