Masculinization of the x chromosome in the pea aphid.

Evolutionary theory predicts that sexually antagonistic mutations accumulate differentially on the X chromosome and autosomes in species with an XY sex-determination system, with effects (masculinization or feminization of the X) depending on the dominance of mutations. Organisms with alternative mo...

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Main Authors: Julie Jaquiéry, Claude Rispe, Denis Roze, Fabrice Legeai, Gaël Le Trionnaire, Solenn Stoeckel, Lucie Mieuzet, Corinne Da Silva, Julie Poulain, Nathalie Prunier-Leterme, Béatrice Ségurens, Denis Tagu, Jean-Christophe Simon
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2013-01-01
Series:PLoS Genetics
Online Access:http://europepmc.org/articles/PMC3738461?pdf=render
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author Julie Jaquiéry
Claude Rispe
Denis Roze
Fabrice Legeai
Gaël Le Trionnaire
Solenn Stoeckel
Lucie Mieuzet
Corinne Da Silva
Julie Poulain
Nathalie Prunier-Leterme
Béatrice Ségurens
Denis Tagu
Jean-Christophe Simon
author_facet Julie Jaquiéry
Claude Rispe
Denis Roze
Fabrice Legeai
Gaël Le Trionnaire
Solenn Stoeckel
Lucie Mieuzet
Corinne Da Silva
Julie Poulain
Nathalie Prunier-Leterme
Béatrice Ségurens
Denis Tagu
Jean-Christophe Simon
author_sort Julie Jaquiéry
collection DOAJ
description Evolutionary theory predicts that sexually antagonistic mutations accumulate differentially on the X chromosome and autosomes in species with an XY sex-determination system, with effects (masculinization or feminization of the X) depending on the dominance of mutations. Organisms with alternative modes of inheritance of sex chromosomes offer interesting opportunities for studying sexual conflicts and their resolution, because expectations for the preferred genomic location of sexually antagonistic alleles may differ from standard systems. Aphids display an XX/X0 system and combine an unusual inheritance of the X chromosome with the alternation of sexual and asexual reproduction. In this study, we first investigated theoretically the accumulation of sexually antagonistic mutations on the aphid X chromosome. Our results show that i) the X is always more favourable to the spread of male-beneficial alleles than autosomes, and should thus be enriched in sexually antagonistic alleles beneficial for males, ii) sexually antagonistic mutations beneficial for asexual females accumulate preferentially on autosomes, iii) in contrast to predictions for standard systems, these qualitative results are not affected by the dominance of mutations. Under the assumption that sex-biased gene expression evolves to solve conflicts raised by the spread of sexually antagonistic alleles, one expects that male-biased genes should be enriched on the X while asexual female-biased genes should be enriched on autosomes. Using gene expression data (RNA-Seq) in males, sexual females and asexual females of the pea aphid, we confirm these theoretical predictions. Although other mechanisms than the resolution of sexual antagonism may lead to sex-biased gene expression, we argue that they could hardly explain the observed difference between X and autosomes. On top of reporting a strong masculinization of the aphid X chromosome, our study highlights the relevance of organisms displaying an alternative mode of sex chromosome inheritance to understanding the forces shaping chromosome evolution.
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spelling doaj.art-44678f5e45f04b63bbd27392866e08732022-12-21T18:47:08ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042013-01-0198e100369010.1371/journal.pgen.1003690Masculinization of the x chromosome in the pea aphid.Julie JaquiéryClaude RispeDenis RozeFabrice LegeaiGaël Le TrionnaireSolenn StoeckelLucie MieuzetCorinne Da SilvaJulie PoulainNathalie Prunier-LetermeBéatrice SégurensDenis TaguJean-Christophe SimonEvolutionary theory predicts that sexually antagonistic mutations accumulate differentially on the X chromosome and autosomes in species with an XY sex-determination system, with effects (masculinization or feminization of the X) depending on the dominance of mutations. Organisms with alternative modes of inheritance of sex chromosomes offer interesting opportunities for studying sexual conflicts and their resolution, because expectations for the preferred genomic location of sexually antagonistic alleles may differ from standard systems. Aphids display an XX/X0 system and combine an unusual inheritance of the X chromosome with the alternation of sexual and asexual reproduction. In this study, we first investigated theoretically the accumulation of sexually antagonistic mutations on the aphid X chromosome. Our results show that i) the X is always more favourable to the spread of male-beneficial alleles than autosomes, and should thus be enriched in sexually antagonistic alleles beneficial for males, ii) sexually antagonistic mutations beneficial for asexual females accumulate preferentially on autosomes, iii) in contrast to predictions for standard systems, these qualitative results are not affected by the dominance of mutations. Under the assumption that sex-biased gene expression evolves to solve conflicts raised by the spread of sexually antagonistic alleles, one expects that male-biased genes should be enriched on the X while asexual female-biased genes should be enriched on autosomes. Using gene expression data (RNA-Seq) in males, sexual females and asexual females of the pea aphid, we confirm these theoretical predictions. Although other mechanisms than the resolution of sexual antagonism may lead to sex-biased gene expression, we argue that they could hardly explain the observed difference between X and autosomes. On top of reporting a strong masculinization of the aphid X chromosome, our study highlights the relevance of organisms displaying an alternative mode of sex chromosome inheritance to understanding the forces shaping chromosome evolution.http://europepmc.org/articles/PMC3738461?pdf=render
spellingShingle Julie Jaquiéry
Claude Rispe
Denis Roze
Fabrice Legeai
Gaël Le Trionnaire
Solenn Stoeckel
Lucie Mieuzet
Corinne Da Silva
Julie Poulain
Nathalie Prunier-Leterme
Béatrice Ségurens
Denis Tagu
Jean-Christophe Simon
Masculinization of the x chromosome in the pea aphid.
PLoS Genetics
title Masculinization of the x chromosome in the pea aphid.
title_full Masculinization of the x chromosome in the pea aphid.
title_fullStr Masculinization of the x chromosome in the pea aphid.
title_full_unstemmed Masculinization of the x chromosome in the pea aphid.
title_short Masculinization of the x chromosome in the pea aphid.
title_sort masculinization of the x chromosome in the pea aphid
url http://europepmc.org/articles/PMC3738461?pdf=render
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