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Repeated Evolution of Asexuality Involves Convergent Gene Expression Changes

Asexual reproduction has evolved repeatedly from sexual ancestors across a wide range of taxa. Whereas the costs and benefits associated with asexuality have received considerable attention, the molecular changes underpinning the evolution of asexual reproduction remain relatively unexplored. In par...

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Autores principales: Parker, Darren J, Bast, Jens, Jalvingh, Kirsten, Dumas, Zoé, Robinson-Rechavi, Marc, Schwander, Tanja
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6404633/
https://www.ncbi.nlm.nih.gov/pubmed/30445505
http://dx.doi.org/10.1093/molbev/msy217
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author Parker, Darren J
Bast, Jens
Jalvingh, Kirsten
Dumas, Zoé
Robinson-Rechavi, Marc
Schwander, Tanja
author_facet Parker, Darren J
Bast, Jens
Jalvingh, Kirsten
Dumas, Zoé
Robinson-Rechavi, Marc
Schwander, Tanja
author_sort Parker, Darren J
collection PubMed
description Asexual reproduction has evolved repeatedly from sexual ancestors across a wide range of taxa. Whereas the costs and benefits associated with asexuality have received considerable attention, the molecular changes underpinning the evolution of asexual reproduction remain relatively unexplored. In particular, it is completely unknown whether the repeated evolution of asexual phenotypes involves similar molecular changes, as previous studies have focused on changes occurring in single lineages. Here, we investigate the extent of convergent gene expression changes across five independent transitions to asexuality in stick insects. We compared gene expression of asexual females to females of close sexual relatives in whole-bodies, reproductive tracts, and legs. We identified a striking amount of convergent gene expression change (up to 8% of genes), greatly exceeding that expected by chance. Convergent changes were also tissue-specific, and most likely driven by selection for functional changes. Genes showing convergent changes in the reproductive tract were associated with meiotic spindle formation and centrosome organization. These genes are particularly interesting as they can influence the production of unreduced eggs, a key barrier to asexual reproduction. Changes in legs and whole-bodies were likely involved in female sexual trait decay, with enrichment in terms such as sperm-storage and pigmentation. By identifying changes occurring across multiple independent transitions to asexuality, our results provide a rare insight into the molecular basis of asexual phenotypes and suggest that the evolutionary path to asexuality is highly constrained, requiring repeated changes to the same key genes.
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spelling pubmed-64046332019-03-12 Repeated Evolution of Asexuality Involves Convergent Gene Expression Changes Parker, Darren J Bast, Jens Jalvingh, Kirsten Dumas, Zoé Robinson-Rechavi, Marc Schwander, Tanja Mol Biol Evol Discoveries Asexual reproduction has evolved repeatedly from sexual ancestors across a wide range of taxa. Whereas the costs and benefits associated with asexuality have received considerable attention, the molecular changes underpinning the evolution of asexual reproduction remain relatively unexplored. In particular, it is completely unknown whether the repeated evolution of asexual phenotypes involves similar molecular changes, as previous studies have focused on changes occurring in single lineages. Here, we investigate the extent of convergent gene expression changes across five independent transitions to asexuality in stick insects. We compared gene expression of asexual females to females of close sexual relatives in whole-bodies, reproductive tracts, and legs. We identified a striking amount of convergent gene expression change (up to 8% of genes), greatly exceeding that expected by chance. Convergent changes were also tissue-specific, and most likely driven by selection for functional changes. Genes showing convergent changes in the reproductive tract were associated with meiotic spindle formation and centrosome organization. These genes are particularly interesting as they can influence the production of unreduced eggs, a key barrier to asexual reproduction. Changes in legs and whole-bodies were likely involved in female sexual trait decay, with enrichment in terms such as sperm-storage and pigmentation. By identifying changes occurring across multiple independent transitions to asexuality, our results provide a rare insight into the molecular basis of asexual phenotypes and suggest that the evolutionary path to asexuality is highly constrained, requiring repeated changes to the same key genes. Oxford University Press 2019-02 2018-11-16 /pmc/articles/PMC6404633/ /pubmed/30445505 http://dx.doi.org/10.1093/molbev/msy217 Text en © The Author(s) 2018. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. http://creativecommons.org/licenses/by/4.0/ This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Discoveries
Parker, Darren J
Bast, Jens
Jalvingh, Kirsten
Dumas, Zoé
Robinson-Rechavi, Marc
Schwander, Tanja
Repeated Evolution of Asexuality Involves Convergent Gene Expression Changes
title Repeated Evolution of Asexuality Involves Convergent Gene Expression Changes
title_full Repeated Evolution of Asexuality Involves Convergent Gene Expression Changes
title_fullStr Repeated Evolution of Asexuality Involves Convergent Gene Expression Changes
title_full_unstemmed Repeated Evolution of Asexuality Involves Convergent Gene Expression Changes
title_short Repeated Evolution of Asexuality Involves Convergent Gene Expression Changes
title_sort repeated evolution of asexuality involves convergent gene expression changes
topic Discoveries
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6404633/
https://www.ncbi.nlm.nih.gov/pubmed/30445505
http://dx.doi.org/10.1093/molbev/msy217
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