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Sexually dimorphic gene expression and transcriptome evolution provide mixed evidence for a fast‐Z effect in Heliconius

Sex chromosomes have different evolutionary properties compared to autosomes due to their hemizygous nature. In particular, recessive mutations are more readily exposed to selection, which can lead to faster rates of molecular evolution. Here, we report patterns of gene expression and molecular evol...

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Autores principales: Pinharanda, Ana, Rousselle, Marjolaine, Martin, Simon H., Hanly, Joe J., Davey, John W., Kumar, Sujai, Galtier, Nicolas, Jiggins, Chris D.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6850379/
https://www.ncbi.nlm.nih.gov/pubmed/30523653
http://dx.doi.org/10.1111/jeb.13410
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author Pinharanda, Ana
Rousselle, Marjolaine
Martin, Simon H.
Hanly, Joe J.
Davey, John W.
Kumar, Sujai
Galtier, Nicolas
Jiggins, Chris D.
author_facet Pinharanda, Ana
Rousselle, Marjolaine
Martin, Simon H.
Hanly, Joe J.
Davey, John W.
Kumar, Sujai
Galtier, Nicolas
Jiggins, Chris D.
author_sort Pinharanda, Ana
collection PubMed
description Sex chromosomes have different evolutionary properties compared to autosomes due to their hemizygous nature. In particular, recessive mutations are more readily exposed to selection, which can lead to faster rates of molecular evolution. Here, we report patterns of gene expression and molecular evolution for a group of butterflies. First, we improve the completeness of the Heliconius melpomene reference annotation, a neotropical butterfly with a ZW sex determination system. Then, we analyse RNA from male and female whole abdomens and sequence female ovary and gut tissue to identify sex‐ and tissue‐specific gene expression profiles in H. melpomene. Using these expression profiles, we compare (a) sequence divergence and polymorphism; (b) the strength of positive and negative selection; and (c) rates of adaptive evolution, for Z and autosomal genes between two species of Heliconius butterflies, H. melpomene and H. erato. We show that the rate of adaptive substitutions is higher for Z than autosomal genes, but contrary to expectation, it is also higher for male‐biased than female‐biased genes. Additionally, we find no significant increase in the rate of adaptive evolution or purifying selection on genes expressed in ovary tissue, a heterogametic‐specific tissue. Our results contribute to a growing body of literature from other ZW systems that also provide mixed evidence for a fast‐Z effect where hemizygosity influences the rate of adaptive substitutions.
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spelling pubmed-68503792019-11-18 Sexually dimorphic gene expression and transcriptome evolution provide mixed evidence for a fast‐Z effect in Heliconius Pinharanda, Ana Rousselle, Marjolaine Martin, Simon H. Hanly, Joe J. Davey, John W. Kumar, Sujai Galtier, Nicolas Jiggins, Chris D. J Evol Biol Research Papers Sex chromosomes have different evolutionary properties compared to autosomes due to their hemizygous nature. In particular, recessive mutations are more readily exposed to selection, which can lead to faster rates of molecular evolution. Here, we report patterns of gene expression and molecular evolution for a group of butterflies. First, we improve the completeness of the Heliconius melpomene reference annotation, a neotropical butterfly with a ZW sex determination system. Then, we analyse RNA from male and female whole abdomens and sequence female ovary and gut tissue to identify sex‐ and tissue‐specific gene expression profiles in H. melpomene. Using these expression profiles, we compare (a) sequence divergence and polymorphism; (b) the strength of positive and negative selection; and (c) rates of adaptive evolution, for Z and autosomal genes between two species of Heliconius butterflies, H. melpomene and H. erato. We show that the rate of adaptive substitutions is higher for Z than autosomal genes, but contrary to expectation, it is also higher for male‐biased than female‐biased genes. Additionally, we find no significant increase in the rate of adaptive evolution or purifying selection on genes expressed in ovary tissue, a heterogametic‐specific tissue. Our results contribute to a growing body of literature from other ZW systems that also provide mixed evidence for a fast‐Z effect where hemizygosity influences the rate of adaptive substitutions. John Wiley and Sons Inc. 2019-01-11 2019-03 /pmc/articles/PMC6850379/ /pubmed/30523653 http://dx.doi.org/10.1111/jeb.13410 Text en © 2018 The Authors. Journal of Evolutionary Biology published by John Wiley & Sons Ltd on behalf of European Society for Evolutionary Biology. This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research Papers
Pinharanda, Ana
Rousselle, Marjolaine
Martin, Simon H.
Hanly, Joe J.
Davey, John W.
Kumar, Sujai
Galtier, Nicolas
Jiggins, Chris D.
Sexually dimorphic gene expression and transcriptome evolution provide mixed evidence for a fast‐Z effect in Heliconius
title Sexually dimorphic gene expression and transcriptome evolution provide mixed evidence for a fast‐Z effect in Heliconius
title_full Sexually dimorphic gene expression and transcriptome evolution provide mixed evidence for a fast‐Z effect in Heliconius
title_fullStr Sexually dimorphic gene expression and transcriptome evolution provide mixed evidence for a fast‐Z effect in Heliconius
title_full_unstemmed Sexually dimorphic gene expression and transcriptome evolution provide mixed evidence for a fast‐Z effect in Heliconius
title_short Sexually dimorphic gene expression and transcriptome evolution provide mixed evidence for a fast‐Z effect in Heliconius
title_sort sexually dimorphic gene expression and transcriptome evolution provide mixed evidence for a fast‐z effect in heliconius
topic Research Papers
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6850379/
https://www.ncbi.nlm.nih.gov/pubmed/30523653
http://dx.doi.org/10.1111/jeb.13410
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