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

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/de...

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Autores principales: Hornett, Emily A., Moran, Bruce, Reynolds, Louise A., Charlat, Sylvain, Tazzyman, Samuel, Wedell, Nina, Jiggins, Chris D., Hurst, Greg D. D.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4256269/
https://www.ncbi.nlm.nih.gov/pubmed/25474676
http://dx.doi.org/10.1371/journal.pgen.1004822
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author Hornett, Emily A.
Moran, Bruce
Reynolds, Louise A.
Charlat, Sylvain
Tazzyman, Samuel
Wedell, Nina
Jiggins, Chris D.
Hurst, Greg D. D.
author_facet Hornett, Emily A.
Moran, Bruce
Reynolds, Louise A.
Charlat, Sylvain
Tazzyman, Samuel
Wedell, Nina
Jiggins, Chris D.
Hurst, Greg D. D.
author_sort Hornett, Emily A.
collection PubMed
description 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.
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spelling pubmed-42562692014-12-11 The Evolution of Sex Ratio Distorter Suppression Affects a 25 cM Genomic Region in the Butterfly Hypolimnas bolina Hornett, Emily A. Moran, Bruce Reynolds, Louise A. Charlat, Sylvain Tazzyman, Samuel Wedell, Nina Jiggins, Chris D. Hurst, Greg D. D. PLoS Genet Research Article 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. Public Library of Science 2014-12-04 /pmc/articles/PMC4256269/ /pubmed/25474676 http://dx.doi.org/10.1371/journal.pgen.1004822 Text en © 2014 Hornett et al http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Hornett, Emily A.
Moran, Bruce
Reynolds, Louise A.
Charlat, Sylvain
Tazzyman, Samuel
Wedell, Nina
Jiggins, Chris D.
Hurst, Greg D. D.
The Evolution of Sex Ratio Distorter Suppression Affects a 25 cM Genomic Region in the Butterfly Hypolimnas bolina
title The Evolution of Sex Ratio Distorter Suppression Affects a 25 cM Genomic Region in the Butterfly Hypolimnas bolina
title_full The Evolution of Sex Ratio Distorter Suppression Affects a 25 cM Genomic Region in the Butterfly Hypolimnas bolina
title_fullStr The Evolution of Sex Ratio Distorter Suppression Affects a 25 cM Genomic Region in the Butterfly Hypolimnas bolina
title_full_unstemmed The Evolution of Sex Ratio Distorter Suppression Affects a 25 cM Genomic Region in the Butterfly Hypolimnas bolina
title_short The Evolution of Sex Ratio Distorter Suppression Affects a 25 cM Genomic Region in the Butterfly Hypolimnas bolina
title_sort evolution of sex ratio distorter suppression affects a 25 cm genomic region in the butterfly hypolimnas bolina
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4256269/
https://www.ncbi.nlm.nih.gov/pubmed/25474676
http://dx.doi.org/10.1371/journal.pgen.1004822
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