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Different Genes are Recruited During Convergent Evolution of Pregnancy and the Placenta

The repeated evolution of the same traits in distantly related groups (convergent evolution) raises a key question in evolutionary biology: do the same genes underpin convergent phenotypes? Here, we explore one such trait, viviparity (live birth), which, qualitative studies suggest, may indeed have...

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Autores principales: Foster, Charles S.P., Van Dyke, James U., Thompson, Michael B., Smith, Nicholas M.A., Simpfendorfer, Colin A., Murphy, Christopher R., Whittington, Camilla M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9048886/
https://www.ncbi.nlm.nih.gov/pubmed/35388432
http://dx.doi.org/10.1093/molbev/msac077
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author Foster, Charles S.P.
Van Dyke, James U.
Thompson, Michael B.
Smith, Nicholas M.A.
Simpfendorfer, Colin A.
Murphy, Christopher R.
Whittington, Camilla M.
author_facet Foster, Charles S.P.
Van Dyke, James U.
Thompson, Michael B.
Smith, Nicholas M.A.
Simpfendorfer, Colin A.
Murphy, Christopher R.
Whittington, Camilla M.
author_sort Foster, Charles S.P.
collection PubMed
description The repeated evolution of the same traits in distantly related groups (convergent evolution) raises a key question in evolutionary biology: do the same genes underpin convergent phenotypes? Here, we explore one such trait, viviparity (live birth), which, qualitative studies suggest, may indeed have evolved via genetic convergence. There are >150 independent origins of live birth in vertebrates, providing a uniquely powerful system to test the mechanisms underpinning convergence in morphology, physiology, and/or gene recruitment during pregnancy. We compared transcriptomic data from eight vertebrates (lizards, mammals, sharks) that gestate embryos within the uterus. Since many previous studies detected qualitative similarities in gene use during independent origins of pregnancy, we expected to find significant overlap in gene use in viviparous taxa. However, we found no more overlap in uterine gene expression associated with viviparity than we would expect by chance alone. Each viviparous lineage exhibits the same core set of uterine physiological functions. Yet, contrary to prevailing assumptions about this trait, we find that none of the same genes are differentially expressed in all viviparous lineages, or even in all viviparous amniote lineages. Therefore, across distantly related vertebrates, different genes have been recruited to support the morphological and physiological changes required for successful pregnancy. We conclude that redundancies in gene function have enabled the repeated evolution of viviparity through recruitment of different genes from genomic “toolboxes”, which are uniquely constrained by the ancestries of each lineage.
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spelling pubmed-90488862022-04-29 Different Genes are Recruited During Convergent Evolution of Pregnancy and the Placenta Foster, Charles S.P. Van Dyke, James U. Thompson, Michael B. Smith, Nicholas M.A. Simpfendorfer, Colin A. Murphy, Christopher R. Whittington, Camilla M. Mol Biol Evol Article The repeated evolution of the same traits in distantly related groups (convergent evolution) raises a key question in evolutionary biology: do the same genes underpin convergent phenotypes? Here, we explore one such trait, viviparity (live birth), which, qualitative studies suggest, may indeed have evolved via genetic convergence. There are >150 independent origins of live birth in vertebrates, providing a uniquely powerful system to test the mechanisms underpinning convergence in morphology, physiology, and/or gene recruitment during pregnancy. We compared transcriptomic data from eight vertebrates (lizards, mammals, sharks) that gestate embryos within the uterus. Since many previous studies detected qualitative similarities in gene use during independent origins of pregnancy, we expected to find significant overlap in gene use in viviparous taxa. However, we found no more overlap in uterine gene expression associated with viviparity than we would expect by chance alone. Each viviparous lineage exhibits the same core set of uterine physiological functions. Yet, contrary to prevailing assumptions about this trait, we find that none of the same genes are differentially expressed in all viviparous lineages, or even in all viviparous amniote lineages. Therefore, across distantly related vertebrates, different genes have been recruited to support the morphological and physiological changes required for successful pregnancy. We conclude that redundancies in gene function have enabled the repeated evolution of viviparity through recruitment of different genes from genomic “toolboxes”, which are uniquely constrained by the ancestries of each lineage. Oxford University Press 2022-04-07 /pmc/articles/PMC9048886/ /pubmed/35388432 http://dx.doi.org/10.1093/molbev/msac077 Text en © The Author(s) 2022. Published by Oxford University Press on behalf of Society for Molecular Biology and Evolution. https://creativecommons.org/licenses/by-nc/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial License (https://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com
spellingShingle Article
Foster, Charles S.P.
Van Dyke, James U.
Thompson, Michael B.
Smith, Nicholas M.A.
Simpfendorfer, Colin A.
Murphy, Christopher R.
Whittington, Camilla M.
Different Genes are Recruited During Convergent Evolution of Pregnancy and the Placenta
title Different Genes are Recruited During Convergent Evolution of Pregnancy and the Placenta
title_full Different Genes are Recruited During Convergent Evolution of Pregnancy and the Placenta
title_fullStr Different Genes are Recruited During Convergent Evolution of Pregnancy and the Placenta
title_full_unstemmed Different Genes are Recruited During Convergent Evolution of Pregnancy and the Placenta
title_short Different Genes are Recruited During Convergent Evolution of Pregnancy and the Placenta
title_sort different genes are recruited during convergent evolution of pregnancy and the placenta
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9048886/
https://www.ncbi.nlm.nih.gov/pubmed/35388432
http://dx.doi.org/10.1093/molbev/msac077
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