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Polyploidy breaks speciation barriers in Australian burrowing frogs Neobatrachus

Polyploidy has played an important role in evolution across the tree of life but it is still unclear how polyploid lineages may persist after their initial formation. While both common and well-studied in plants, polyploidy is rare in animals and generally less understood. The Australian burrowing f...

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Autores principales: Novikova, Polina Yu., Brennan, Ian G., Booker, William, Mahony, Michael, Doughty, Paul, Lemmon, Alan R., Moriarty Lemmon, Emily, Roberts, J. Dale, Yant, Levi, Van de Peer, Yves, Keogh, J. Scott, Donnellan, Stephen C.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7259803/
https://www.ncbi.nlm.nih.gov/pubmed/32392206
http://dx.doi.org/10.1371/journal.pgen.1008769
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author Novikova, Polina Yu.
Brennan, Ian G.
Booker, William
Mahony, Michael
Doughty, Paul
Lemmon, Alan R.
Moriarty Lemmon, Emily
Roberts, J. Dale
Yant, Levi
Van de Peer, Yves
Keogh, J. Scott
Donnellan, Stephen C.
author_facet Novikova, Polina Yu.
Brennan, Ian G.
Booker, William
Mahony, Michael
Doughty, Paul
Lemmon, Alan R.
Moriarty Lemmon, Emily
Roberts, J. Dale
Yant, Levi
Van de Peer, Yves
Keogh, J. Scott
Donnellan, Stephen C.
author_sort Novikova, Polina Yu.
collection PubMed
description Polyploidy has played an important role in evolution across the tree of life but it is still unclear how polyploid lineages may persist after their initial formation. While both common and well-studied in plants, polyploidy is rare in animals and generally less understood. The Australian burrowing frog genus Neobatrachus is comprised of six diploid and three polyploid species and offers a powerful animal polyploid model system. We generated exome-capture sequence data from 87 individuals representing all nine species of Neobatrachus to investigate species-level relationships, the origin and inheritance mode of polyploid species, and the population genomic effects of polyploidy on genus-wide demography. We describe rapid speciation of diploid Neobatrachus species and show that the three independently originated polyploid species have tetrasomic or mixed inheritance. We document higher genetic diversity in tetraploids, resulting from widespread gene flow between the tetraploids, asymmetric inter-ploidy gene flow directed from sympatric diploids to tetraploids, and isolation of diploid species from each other. We also constructed models of ecologically suitable areas for each species to investigate the impact of climate on differing ploidy levels. These models suggest substantial change in suitable areas compared to past climate, which correspond to population genomic estimates of demographic histories. We propose that Neobatrachus diploids may be suffering the early genomic impacts of climate-induced habitat loss, while tetraploids appear to be avoiding this fate, possibly due to widespread gene flow. Finally, we demonstrate that Neobatrachus is an attractive model to study the effects of ploidy on the evolution of adaptation in animals.
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spelling pubmed-72598032020-06-02 Polyploidy breaks speciation barriers in Australian burrowing frogs Neobatrachus Novikova, Polina Yu. Brennan, Ian G. Booker, William Mahony, Michael Doughty, Paul Lemmon, Alan R. Moriarty Lemmon, Emily Roberts, J. Dale Yant, Levi Van de Peer, Yves Keogh, J. Scott Donnellan, Stephen C. PLoS Genet Research Article Polyploidy has played an important role in evolution across the tree of life but it is still unclear how polyploid lineages may persist after their initial formation. While both common and well-studied in plants, polyploidy is rare in animals and generally less understood. The Australian burrowing frog genus Neobatrachus is comprised of six diploid and three polyploid species and offers a powerful animal polyploid model system. We generated exome-capture sequence data from 87 individuals representing all nine species of Neobatrachus to investigate species-level relationships, the origin and inheritance mode of polyploid species, and the population genomic effects of polyploidy on genus-wide demography. We describe rapid speciation of diploid Neobatrachus species and show that the three independently originated polyploid species have tetrasomic or mixed inheritance. We document higher genetic diversity in tetraploids, resulting from widespread gene flow between the tetraploids, asymmetric inter-ploidy gene flow directed from sympatric diploids to tetraploids, and isolation of diploid species from each other. We also constructed models of ecologically suitable areas for each species to investigate the impact of climate on differing ploidy levels. These models suggest substantial change in suitable areas compared to past climate, which correspond to population genomic estimates of demographic histories. We propose that Neobatrachus diploids may be suffering the early genomic impacts of climate-induced habitat loss, while tetraploids appear to be avoiding this fate, possibly due to widespread gene flow. Finally, we demonstrate that Neobatrachus is an attractive model to study the effects of ploidy on the evolution of adaptation in animals. Public Library of Science 2020-05-11 /pmc/articles/PMC7259803/ /pubmed/32392206 http://dx.doi.org/10.1371/journal.pgen.1008769 Text en © 2020 Novikova et al 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 use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Novikova, Polina Yu.
Brennan, Ian G.
Booker, William
Mahony, Michael
Doughty, Paul
Lemmon, Alan R.
Moriarty Lemmon, Emily
Roberts, J. Dale
Yant, Levi
Van de Peer, Yves
Keogh, J. Scott
Donnellan, Stephen C.
Polyploidy breaks speciation barriers in Australian burrowing frogs Neobatrachus
title Polyploidy breaks speciation barriers in Australian burrowing frogs Neobatrachus
title_full Polyploidy breaks speciation barriers in Australian burrowing frogs Neobatrachus
title_fullStr Polyploidy breaks speciation barriers in Australian burrowing frogs Neobatrachus
title_full_unstemmed Polyploidy breaks speciation barriers in Australian burrowing frogs Neobatrachus
title_short Polyploidy breaks speciation barriers in Australian burrowing frogs Neobatrachus
title_sort polyploidy breaks speciation barriers in australian burrowing frogs neobatrachus
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7259803/
https://www.ncbi.nlm.nih.gov/pubmed/32392206
http://dx.doi.org/10.1371/journal.pgen.1008769
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