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.

Host genotype changes bidirectional to unidirectional cytoplasmic incompatibility in Nasonia longicornis

“…They found that the bi-CI between two strains, Bei and Pel, was lost when the latter's genome was introgressed into the former's cytoplasm. Theoretical studies predict that host suppressors of incompatibility will be selected for (Rousset et al, 1991;Turelli, 1994;Koehncke et al, 2009) and there are recent examples of such repressors being found in nature (Hornett et al, 2006). Koehncke et al (2009) showed theoretically that selection particularly favors the evolution of nuclear suppressors of sperm modification in males, because such genotypes are reproductively compatible with both infected and uninfected types.…”

Incomplete offspring sex bias in Australian populations of the butterfly Eurema hecabe

“…Although not always maladaptive for hosts, these manipulations often create misalignments of evolutionary interests that, in turn, set the scene for host-endosymbiont coevolution (Riegler and O'Neill, 2007;Cordaux et al, 2011). Documented host counteradaptations include nuclear suppressors that restore the viability and/or natural phenotypic development of male genotypes (Hornett et al, 2006;Charlat et al, 2007b).…”

“…Lepidoptera have proven an excellent group for exploring arthropodendosymbiont dynamics (Dyson and Hurst, 2004;Hornett et al, 2006;Sugimoto and Ishikawa, 2012). This group harbors bacterial symbionts such as Spiroplasma and Wolbachia collectively known to impose CI, male killing and feminization (Jiggins et al, 2000;Hiroki et al, 2004;Charlat et al, 2005).…”

“…This group harbors bacterial symbionts such as Spiroplasma and Wolbachia collectively known to impose CI, male killing and feminization (Jiggins et al, 2000;Hiroki et al, 2004;Charlat et al, 2005). Studies of butterfly male-killing have yielded valuable insights into host-symbiont coadaptation, including the genetic and biogeographic basis of nuclear host suppression (Dyson and Hurst, 2004;Hornett et al, 2006Hornett et al, , 2008Charlat et al, 2007b, c). Lepidopterans have also informed the study of feminization, primarily via the work in Wolbachia-infected Ostrinia moths (Crambidae) and Eurema butterflies (Pieridae).…”

Essential but unhelpful wasp Wolbachia

“…Recently, it has become apparent that Wolbachia infections influence the fitness of their hosts in diverse ways, by altering patterns of reproduction, resistance to microbial infections and the provision of nutrients (Hedges et al, 2008;Teixeira et al, 2008;Ghedin et al, 2008). Changes in Wolbachia or their host genomes in the same species have now been documented (Hornett et al, 2006;Weeks et al, 2007) and suggest that evolutionary shifts in Wolbachia-host interactions (and their host effects) can be rapid. Wolbachia can therefore mediate rapid evolutionary shifts in host reproductive patterns and fitness effects.…”