Extraordinarily wide genomic impact of a selective sweep associated with the evolution of sex ratio distorter suppression

Abstract

Symbionts that distort their hosts sex ratio by favouring the production and survival of females are common in arthropods. Their presence produces intense Fisherian selection to return the sex ratio to parity, typified by the rapid spread of host suppressor loci that restore male survival/development. In this study, we investigated the genomic impact of a selective event of this kind in the butterfly Hypolimnas bolina. Through linkage mapping we first identified a genomic region that was necessary for males to survive Wolbachia-induced killing. We then investigated the genomic impact of the rapid spread of suppression that converted the Samoan population of this butterfly from a 100:1 female-biased sex ratio in 2001, to a 1:1 sex ratio by 2006. Models of this process revealed the potential for a chromosome-wide selective sweep. To measure the impact directly, the pattern of genetic variation before and after the episode of selection was compared. Significant changes in allele frequencies were observed over a 25cM region surrounding the suppressor locus, alongside generation of linkage disequilibrium. The presence of novel allelic variants in 2006 suggests that the suppressor was introduced via immigration rather than through de novo mutation. In addition, further sampling in 2010 indicated that many of the introduced variants were lost or had reduced in frequency since 2006. We hypothesise that this loss may have resulted from a period of purifying selection - removing deleterious material that introgressed during the initial sweep. Our observations of the impact of suppression of sex ratio distorting activity reveal an extraordinarily wide genomic imprint, reflecting its status as one of the strongest selective forces in nature.