Evolution of Male-Killer Suppression in a Natural Population

Emily A Hornett,Nina Wedell,Gregory D D Hurst,Anne M R Duplouy,George K Roderick,Laurent Keller,Sylvain Charlat,Neil Davies

doi:10.1371/journal.pbio.0040283

Abstract

Male-killing bacteria are widespread in arthropods, and can profoundly alter the reproductive biology of their host species. Here we detail the first case of complete suppression of a male killer. The nymphalid butterfly Hypolimnas bolina is infected with a strain of the bacterium Wolbachia, wBol1, which kills male host embryos in Polynesian populations, but does not do so in many areas of Southeast Asia, where both males and female adults are naturally infected, and wBol1-infected females produce a 1:1 sex ratio. We demonstrate that absence of male killing by wBol1 is associated with dominant zygotic suppression of the action of the male killer. Simulations demonstrate host suppressors of male-killer action can spread very rapidly, and historical data indicating the presence of male killing in Southeast Asia in the very recent past suggests suppressor spread has been a very recent occurrence. Thus, male killer/host interactions are much more dynamic than previously recognised, with rapid and dramatic loss of the phenotype. Our results also indicate that suppression can render male killers completely quiescent, leading to the conclusion that some species that do not currently express a male killer may have done so in the past, and thus that more species have had their biology affected by these parasites than previously believed.

Highlights

Selfish genetic elements that distort the sex ratio of their host were first recorded over 80 y ago [1]
In the past 3 y, we have obtained four Thai and two Philippine stocks all derived independently from the wild, two generations ago. The origins of these stocks flank the previously observed populations to the East and West geographically, and all stocks displayed the same pattern as other Southeast Asian material: females were infected with wBol1, eggs laid had a high egg hatch rate, and the broods produced had a 1:1 sex ratio, with resulting males infected
In order to test for the role of host suppressor genes in causing phenotypic differences in Wolbachia infection, we investigated a) whether wBol1 isolates from Moorea, known to be competent for male killing, retain or lose this ability on a Thai/Philippine nuclear genetic background; and, b) whether wBol1 isolates from Thailand/Philippines, that currently do not kill males, do so when placed on a Moorean nuclear genetic background

Summary

Introduction

Selfish genetic elements that distort the sex ratio of their host were first recorded over 80 y ago [1]. In creating sex ratio distortion, these elements increase the fitness of individuals producing the rare sex [4] They select for unlinked modifiers within the host genome that suppress the action or reduce the transmission efficiency of the sex ratio-distorting element, restoring the sex ratio to unity [5]. Evidence for this co-evolutionary ‘‘struggle’’ between sex ratio-distorting elements and their hosts is provided by studies of both sex chromosome meiotic drive [6] and cytoplasmic male sterility [7]. The majority of these sex ratio-distorting elements are found in the presence of host suppressors that inhibit their action [7,8]

Methods

Results

Conclusion