title: The evolution of sex ratio distorter suppression affects a 25 cM genomic region in the butterfly Hypolimnas bolina.
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.
authors.affiliation: Institute of Integrative Biology, University of Liverpool, Liverpool, United Kingdom; Department of Zoology, University of Cambridge, Cambridge, United Kingdom.
authors.forename: Emily A
authors.initials: EA
authors.lastname: Hornett
authors.affiliation: Institute of Integrative Biology, University of Liverpool, Liverpool, United Kingdom.
authors.forename: Bruce
authors.initials: B
authors.lastname: Moran
authors.affiliation: Institute of Integrative Biology, University of Liverpool, Liverpool, United Kingdom.
authors.forename: Louise A
authors.initials: LA
authors.lastname: Reynolds
authors.affiliation: Laboratory of Biometry and Evolutionary Biology, CNRS - University Lyon, Villeurbanne, France.
authors.forename: Sylvain
authors.initials: S
authors.lastname: Charlat
authors.affiliation: Faculty of Life Sciences, University College London, London, United Kingdom; Theoretical Biology, ETH Zürich, Zürich, Switzerland.
authors.forename: Samuel
authors.initials: S
authors.lastname: Tazzyman
authors.affiliation: Centre for Ecology and Conservation, University of Exeter, Penryn, United Kingdom.
authors.forename: Nina
authors.initials: N
authors.lastname: Wedell
authors.affiliation: Department of Zoology, University of Cambridge, Cambridge, United Kingdom.
authors.forename: Chris D
authors.initials: CD
authors.lastname: Jiggins
authors.affiliation: Institute of Integrative Biology, University of Liverpool, Liverpool, United Kingdom.
authors.forename: Greg D D
authors.initials: GD
authors.lastname: Hurst
mesh_terms: D000818:Animals; D002080:Butterflies / Q000235:genetics*; D019143:Evolution, Molecular; D005260:Female; D014644:Genetic Variation; D049750:Genome, Insect / Q000235:genetics*; D016905:Gram-Negative Bacterial Infections / Q000235:genetics / Q000662:veterinary; D054884:Host-Pathogen Interactions / Q000235:genetics*; D015810:Linkage Disequilibrium; D008297:Male; D008969:Molecular Sequence Data; D018947:Samoa; D012744:Sex Ratio; D013489:Suppression, Genetic; D020577:Wolbachia / Q000235:genetics / Q000472:pathogenicity