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Section: Evolutionary Biology
Topic: Evolution, Genetics/Genomics, Population biology

Masculinization of the X-chromosome in aphid soma and gonads

Jaquiéry, Julie1  ; Simon, Jean-Christophe1 ; Robin, Stéphanie1, 2 ; Richard, Gautier1; Peccoud, Jean3 ; Boulain, Hélène4; Legeai, Fabrice1, 2 ; Tanguy, Sylvie1; Prunier-Leterme, Nathalie1; Letrionnaire, Gaël1
1 INRAE, UMR 1349, Institute of Genetics, Environment and Plant Protection - Le Rheu, France
2 University of Rennes, CNRS, Inria, IRISA, UMR 6074 - Rennes, France
3 Laboratoire Ecologie et Biologie des Interactions, Equipe Ecologie Evolution Symbiose, UMR CNRS 7267, Université de Poitiers - Poitiers, France
4 Department of Ecology and Evolution, University of Lausanne - Lausanne, Switzerland

10.24072/pcjournal.166 - Peer Community Journal, Volume 2 (2022), article no. e53.

Get full text PDF Peer reviewed and recommended by PCI

Males and females share essentially the same genome but differ in their optimal values for many phenotypic traits, which can result in intra-locus conflict between the sexes. Aphids display XX/X0 sex chromosomes and combine unusual X chromosome inheritance with cyclical parthenogenesis. Theoretical and empirical works support the hypothesis that the large excess of male-biased genes observed on the aphid X chromosome compared to autosomes evolved in response to sexual conflicts, by restricting the products of sexually antagonistic alleles to the sex they benefits. However, whether such masculinization of the X affects all tissues (as expected if it evolved in response to sexual conflicts) or is limited to specific tissues remains an open question. Here, we measured gene expression in three different somatic and gonadic tissues of males, sexual females and parthenogenetic females of the pea aphid. We observed a masculinization of the X in each of the studied tissues, with male-biased genes being 2.5 to 3.5 more frequent on the X than expected. We also tested the hypothesis that gene duplication can facilitate the attenuation of conflicts by allowing gene copies to neo- or sub-functionalize and reach sex-specific optima. As predicted, X-linked copies of duplicated genes having their other copies on autosomes were more frequently male-biased (40.5% of the genes) than duplicated autosomal genes (6.6%) or X-linked single-copy genes (32.5%). These results highlight a peculiar pattern of expression of X-linked genes in aphids at the tissue level and provide further support for sex-biased expression as a mechanism to attenuate intra-locus sexual conflicts.

Published online:
DOI: 10.24072/pcjournal.166
Type: Research article
Jaquiéry, Julie 1; Simon, Jean-Christophe 1; Robin, Stéphanie 1, 2; Richard, Gautier 1; Peccoud, Jean 3; Boulain, Hélène 4; Legeai, Fabrice 1, 2; Tanguy, Sylvie 1; Prunier-Leterme, Nathalie 1; Letrionnaire, Gaël 1

1 INRAE, UMR 1349, Institute of Genetics, Environment and Plant Protection - Le Rheu, France
2 University of Rennes, CNRS, Inria, IRISA, UMR 6074 - Rennes, France
3 Laboratoire Ecologie et Biologie des Interactions, Equipe Ecologie Evolution Symbiose, UMR CNRS 7267, Université de Poitiers - Poitiers, France
4 Department of Ecology and Evolution, University of Lausanne - Lausanne, Switzerland
License: CC-BY 4.0
Copyrights: The authors retain unrestricted copyrights and publishing rights 
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     title = {Masculinization of the {X-chromosome} in aphid soma and gonads},
     journal = {Peer Community Journal},
     eid = {e53},
     publisher = {Peer Community In},
     volume = {2},
     year = {2022},
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     url = {https://peercommunityjournal.org/articles/10.24072/pcjournal.166/}
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Jaquiéry, Julie; Simon, Jean-Christophe; Robin, Stéphanie; Richard, Gautier; Peccoud, Jean; Boulain, Hélène; Legeai, Fabrice; Tanguy, Sylvie; Prunier-Leterme, Nathalie; Letrionnaire, Gaël. Masculinization of the X-chromosome in aphid soma and gonads. Peer Community Journal, Volume 2 (2022), article  no. e53. doi : 10.24072/pcjournal.166. https://peercommunityjournal.org/articles/10.24072/pcjournal.166/

Peer reviewed and recommended by PCI : 10.24072/pci.evolbiol.100148

Conflict of interest of the recommender and peer reviewers:
The recommender in charge of the evaluation of the article and the reviewers declared that they have no conflict of interest (as defined in the code of conduct of PCI) with the authors or with the content of the article.

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