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Variable dosage compensation is associated with female consequences of an X-linked, male-beneficial mutation

Recent theory has suggested that dosage compensation mediates sexual antagonism over X-linked genes. This process relies on the assumption that dosage compensation scales phenotypic effects between the sexes, which is largely untested. We evaluated this by quantifying transcriptome variation associa...

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Autores principales: Rayner, Jack G., Hitchcock, Thomas J., Bailey, Nathan W.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The Royal Society 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8059673/
https://www.ncbi.nlm.nih.gov/pubmed/33757350
http://dx.doi.org/10.1098/rspb.2021.0355
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author Rayner, Jack G.
Hitchcock, Thomas J.
Bailey, Nathan W.
author_facet Rayner, Jack G.
Hitchcock, Thomas J.
Bailey, Nathan W.
author_sort Rayner, Jack G.
collection PubMed
description Recent theory has suggested that dosage compensation mediates sexual antagonism over X-linked genes. This process relies on the assumption that dosage compensation scales phenotypic effects between the sexes, which is largely untested. We evaluated this by quantifying transcriptome variation associated with a recently arisen, male-beneficial, X-linked mutation across tissues of the field cricket Teleogryllus oceanicus, and testing the relationship between the completeness of dosage compensation and female phenotypic effects at the level of gene expression. Dosage compensation in T. oceanicus was variable across tissues but usually incomplete, such that relative expression of X-linked genes was typically greater in females. Supporting the assumption that dosage compensation scales phenotypic effects between the sexes, we found tissues with incomplete dosage compensation tended to show female-skewed effects of the X-linked allele. In gonads, where expression of X-linked genes was most strongly female-biased, ovaries-limited genes were much more likely to be X-linked than were testes-limited genes, supporting the view that incomplete dosage compensation favours feminization of the X. Our results support the expectation that sex chromosome dosage compensation scales phenotypic effects of X-linked genes between sexes, substantiating a key assumption underlying the theoretical role of dosage compensation in determining the dynamics of sexual antagonism on the X.
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spelling pubmed-80596732021-06-01 Variable dosage compensation is associated with female consequences of an X-linked, male-beneficial mutation Rayner, Jack G. Hitchcock, Thomas J. Bailey, Nathan W. Proc Biol Sci Evolution Recent theory has suggested that dosage compensation mediates sexual antagonism over X-linked genes. This process relies on the assumption that dosage compensation scales phenotypic effects between the sexes, which is largely untested. We evaluated this by quantifying transcriptome variation associated with a recently arisen, male-beneficial, X-linked mutation across tissues of the field cricket Teleogryllus oceanicus, and testing the relationship between the completeness of dosage compensation and female phenotypic effects at the level of gene expression. Dosage compensation in T. oceanicus was variable across tissues but usually incomplete, such that relative expression of X-linked genes was typically greater in females. Supporting the assumption that dosage compensation scales phenotypic effects between the sexes, we found tissues with incomplete dosage compensation tended to show female-skewed effects of the X-linked allele. In gonads, where expression of X-linked genes was most strongly female-biased, ovaries-limited genes were much more likely to be X-linked than were testes-limited genes, supporting the view that incomplete dosage compensation favours feminization of the X. Our results support the expectation that sex chromosome dosage compensation scales phenotypic effects of X-linked genes between sexes, substantiating a key assumption underlying the theoretical role of dosage compensation in determining the dynamics of sexual antagonism on the X. The Royal Society 2021-03-31 2021-03-24 /pmc/articles/PMC8059673/ /pubmed/33757350 http://dx.doi.org/10.1098/rspb.2021.0355 Text en © 2021 The Authors. https://creativecommons.org/licenses/by/4.0/Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, provided the original author and source are credited.
spellingShingle Evolution
Rayner, Jack G.
Hitchcock, Thomas J.
Bailey, Nathan W.
Variable dosage compensation is associated with female consequences of an X-linked, male-beneficial mutation
title Variable dosage compensation is associated with female consequences of an X-linked, male-beneficial mutation
title_full Variable dosage compensation is associated with female consequences of an X-linked, male-beneficial mutation
title_fullStr Variable dosage compensation is associated with female consequences of an X-linked, male-beneficial mutation
title_full_unstemmed Variable dosage compensation is associated with female consequences of an X-linked, male-beneficial mutation
title_short Variable dosage compensation is associated with female consequences of an X-linked, male-beneficial mutation
title_sort variable dosage compensation is associated with female consequences of an x-linked, male-beneficial mutation
topic Evolution
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8059673/
https://www.ncbi.nlm.nih.gov/pubmed/33757350
http://dx.doi.org/10.1098/rspb.2021.0355
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