Suppression ofWolbachia-mediated male-killing in the butterflyHypolimnas bolinainvolves a single genomic region

Abstract

Background Sex ratio distorting agents (maternally inherited symbionts and meiotically-driving sex chromosomes) are common in insects. When these agents rise to high frequencies they create strong population sex ratio bias and selection then favours mutations that act to restore the rare sex. Despite this strong selection pressure, the evolution of mutations that suppress sex ratio distorting elements appears to be constrained in many cases, where sex-biased populations persist for many generations. This scenario has been observed in the butterfly Hypolimnas bolina, where Wolbachia-mediated male killing endured for 800–1,000 generations across multiple populations before the evolution of suppression. Here we test the hypothesis that this evolutionary lag is the result of suppression being a multilocus trait requiring multiple mutations. Methods We developed genetic markers, based on conservation of synteny, for each H. bolina chromosome and verified coverage using recombinational mapping. We then used a Wolbachia-infected mapping family to assess each chromosome for the presence of loci required for male survival, as determined by the presence of markers in all surviving sons. Results Informative markers were obtained for each of the 31 chromosomes in H. bolina. The only marker that cosegregated with suppression was located on chromosome 25. A genomic region necessary for suppression has previously been located on this chromosome. We therefore conclude that a single genomic region of the H. bolina genome is necessary for male-killing suppression. Discussion The evolutionary lag observed in our system is not caused by a need for changes at multiple genomic locations. The findings favour hypotheses in which either multiple mutations are required within a single genomic region, or the suppressor mutation is a singularly rare event.

The Wolbachia cytoplasmic incompatibility enzyme CidB targets nuclear import and protamine-histone exchange factors

“…Host suppression of reproductive parasitism has been documented in multiple Wolbachia systems involving CI (Cooper et al, 2017) and male killing (Hornett et al, 2006; Reynolds et al, 2019). Theory predicts that CI will progressively evolve to weaker incompatibilities (Turelli, 1994; Prout, 1994).…”

Sex determination systems as the interface between male-killing bacteria and their hosts

“…Data from the introgression experiments described above are compatible with the suppressor being controlled at a single locus. Further investigation revealed that only one genomic region is necessary for males to survive w Bol1-induced MK [ 42 ]. Uniquely in this system, data of the suppressor locus has been combined with the real-time observation of natural selection in Samoa, to allow study of the genomic impact of the rapid spread of the suppressor.…”

Wolbachiahost shifts: routes, mechanisms, constraints and evolutionary consequences

“…This seems to stem from a recent amino acid substitution in this gene, since no such phenomenon is seen in the close relative Nasonia giraulti (Funkhouser-Jones and van Opstal et al 2018). Male killing suppression in H. bolina butterflies offers another example of a derived and recent mechanism, stemming in that case from one or more mutations in a single host genomic region (Reynolds et al, 2019). These studies indicate that rather than being polygenic and conserved ancestral traits, host resistance may often be strain-and host-specific control systems that evolved very recently, and with a simple genetic basis.…”