Evolution of male-killer suppression in a natural population

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.

Figure 1. Sex Ratio Produced by wBol1-Infected Females during Introgression onto Different Host Genetic Backgrounds

(A) The mean sex ratio (proportion male) produced by wBol1 infected H. bolina derived from the Moorean matriline 595 on introgression onto a Phi ‘05 nuclear background over three generations. Solid black: introgression onto a Phi ‘05 nuclear background; dashed black: backcross to Moorean males; grey triangles: Phi ‘05 control; grey squares: Moorean matriline 595 control. (B) As above, for the Moorean 787 wBol1 isolate introgressed onto a Thai '05 nuclear background. Solid black: introgression; dashed black: backcross to Moorean males; grey triangles: Thai ‘05 control; grey squares: Moorean matriline 787 control. (C) The sex ratio (proportion male) produced by wBol1 infected H. bolina derived from the Philippines (Phi '05) on introgression onto a Moorean nuclear background over 3 generations. Solid black: introgression; dashed black: backcross to Moorean males; grey triangles: Phi ‘05 control; grey squares: Moorean control. (D) As above, for the Thai ‘05 infection introgressed onto a Moorean nuclear background. Solid black: introgression; grey triangles: Thai '05 control; grey squares: Moorean control. Samples sizes and number of crosses performed are given in text and in Tables 1 and 2.

Figure 2. Time of Spread of the Male-Killing Suppressor with Varying Initial Male Killer Prevalence

Time (given as the number of host generations) taken to spread from 1% to 95% frequency for a zygotically acting, single locus dominant suppressor of male killing, with varying initial prevalence of male-killing wBol1 strain. Results are derived from simulation of gene frequency changes for varying initial prevalence of wBol1 (given in Protocol S1), with the assumption that wBol1 shows perfect vertical transmission and no direct benefit or cost to the female host, save death of male offspring. The simulation assumes the suppressor rescues males completely, is fully penetrant, and has no direct cost. Code for the recursions is available on request.