The Evolution of Sex Ratio Distorter Suppression Affects a 25 cM Genomic Region in the Butterfly Hypolimnas bolina

Hornett, Emily, Moran, Bruce, Reynolds, Louise, Charlat, Sylvain, Tazzyman, Samuel, Wedell, Nina, Jiggins, Chris D and Hurst, Greg ORCID: 0000-0002-7163-7784 (2014) The Evolution of Sex Ratio Distorter Suppression Affects a 25 cM Genomic Region in the Butterfly Hypolimnas bolina. PLoS Genetics, 10 (12). e1004822-.

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Abstract

Symbionts that distort their host's 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 male-killing. We then investigated the genomic impact of the rapid spread of suppression, which 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 effect. To measure the impact of this episode of selection directly, the pattern of genetic variation before and after the spread of suppression was compared. Changes in allele frequencies were observed over a 25 cM region surrounding the suppressor locus, with a reduction in overall diversity observed at loci that co-segregate with the suppressor. These changes exceeded those expected from drift and occurred alongside the generation of linkage disequilibrium. The presence of novel allelic variants in 2006 suggests that the suppressor was likely to have been 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 declined in frequency since 2006. We hypothesize 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 a very wide genomic imprint, reflecting its status as one of the strongest selective forces in nature.

Item Type:	Article
Uncontrolled Keywords:	Animals, Butterflies, Wolbachia, Gram-Negative Bacterial Infections, Sex Ratio, Evolution, Molecular, Suppression, Genetic, Linkage Disequilibrium, Molecular Sequence Data, Samoa, Female, Male, Genome, Insect, Host-Pathogen Interactions, Genetic Variation
Depositing User:	Symplectic Admin
Date Deposited:	11 Mar 2015 10:45
Last Modified:	15 Dec 2022 12:08
DOI:	10.1371/journal.pgen.1004822
Related URLs:	Author Publisher
URI:	https://livrepository.liverpool.ac.uk/id/eprint/2008021