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The Complex History of Genome Duplication and Hybridization in North American Gray Treefrogs

Polyploid speciation has played an important role in evolutionary history across the tree of life, yet there remain large gaps in our understanding of how polyploid species form and persist. Although systematic studies have been conducted in numerous polyploid complexes, recent advances in sequencin...

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Autores principales: Booker, William W, Gerhardt, H Carl, Lemmon, Alan R, Ptacek, Margaret B, Hassinger, Alyssa T B, Schul, Johannes, Lemmon, Emily Moriarty
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8826561/
https://www.ncbi.nlm.nih.gov/pubmed/34791374
http://dx.doi.org/10.1093/molbev/msab316
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author Booker, William W
Gerhardt, H Carl
Lemmon, Alan R
Ptacek, Margaret B
Hassinger, Alyssa T B
Schul, Johannes
Lemmon, Emily Moriarty
author_facet Booker, William W
Gerhardt, H Carl
Lemmon, Alan R
Ptacek, Margaret B
Hassinger, Alyssa T B
Schul, Johannes
Lemmon, Emily Moriarty
author_sort Booker, William W
collection PubMed
description Polyploid speciation has played an important role in evolutionary history across the tree of life, yet there remain large gaps in our understanding of how polyploid species form and persist. Although systematic studies have been conducted in numerous polyploid complexes, recent advances in sequencing technology have demonstrated that conclusions from data-limited studies may be spurious and misleading. The North American gray treefrog complex, consisting of the diploid Hyla chrysoscelis and the tetraploid H. versicolor, has long been used as a model system in a variety of biological fields, yet all taxonomic studies to date were conducted with only a few loci from nuclear and mitochondrial genomes. Here, we utilized anchored hybrid enrichment and high-throughput sequencing to capture hundreds of loci along with whole mitochondrial genomes to investigate the evolutionary history of this complex. We used several phylogenetic and population genetic methods, including coalescent simulations and testing of polyploid speciation models with approximate Bayesian computation, to determine that H. versicolor was most likely formed via autopolyploidization from a now extinct lineage of H. chrysoscelis. We also uncovered evidence of significant hybridization between diploids and tetraploids where they co-occur, and show that historical hybridization between these groups led to the re-formation of distinct polyploid lineages following the initial whole-genome duplication event. Our study indicates that a wide variety of methods and explicit model testing of polyploid histories can greatly facilitate efforts to uncover the evolutionary history of polyploid complexes.
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spelling pubmed-88265612022-02-09 The Complex History of Genome Duplication and Hybridization in North American Gray Treefrogs Booker, William W Gerhardt, H Carl Lemmon, Alan R Ptacek, Margaret B Hassinger, Alyssa T B Schul, Johannes Lemmon, Emily Moriarty Mol Biol Evol Discoveries Polyploid speciation has played an important role in evolutionary history across the tree of life, yet there remain large gaps in our understanding of how polyploid species form and persist. Although systematic studies have been conducted in numerous polyploid complexes, recent advances in sequencing technology have demonstrated that conclusions from data-limited studies may be spurious and misleading. The North American gray treefrog complex, consisting of the diploid Hyla chrysoscelis and the tetraploid H. versicolor, has long been used as a model system in a variety of biological fields, yet all taxonomic studies to date were conducted with only a few loci from nuclear and mitochondrial genomes. Here, we utilized anchored hybrid enrichment and high-throughput sequencing to capture hundreds of loci along with whole mitochondrial genomes to investigate the evolutionary history of this complex. We used several phylogenetic and population genetic methods, including coalescent simulations and testing of polyploid speciation models with approximate Bayesian computation, to determine that H. versicolor was most likely formed via autopolyploidization from a now extinct lineage of H. chrysoscelis. We also uncovered evidence of significant hybridization between diploids and tetraploids where they co-occur, and show that historical hybridization between these groups led to the re-formation of distinct polyploid lineages following the initial whole-genome duplication event. Our study indicates that a wide variety of methods and explicit model testing of polyploid histories can greatly facilitate efforts to uncover the evolutionary history of polyploid complexes. Oxford University Press 2021-11-13 /pmc/articles/PMC8826561/ /pubmed/34791374 http://dx.doi.org/10.1093/molbev/msab316 Text en © The Author(s) 2021. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. https://creativecommons.org/licenses/by/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://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
Booker, William W
Gerhardt, H Carl
Lemmon, Alan R
Ptacek, Margaret B
Hassinger, Alyssa T B
Schul, Johannes
Lemmon, Emily Moriarty
The Complex History of Genome Duplication and Hybridization in North American Gray Treefrogs
title The Complex History of Genome Duplication and Hybridization in North American Gray Treefrogs
title_full The Complex History of Genome Duplication and Hybridization in North American Gray Treefrogs
title_fullStr The Complex History of Genome Duplication and Hybridization in North American Gray Treefrogs
title_full_unstemmed The Complex History of Genome Duplication and Hybridization in North American Gray Treefrogs
title_short The Complex History of Genome Duplication and Hybridization in North American Gray Treefrogs
title_sort complex history of genome duplication and hybridization in north american gray treefrogs
topic Discoveries
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8826561/
https://www.ncbi.nlm.nih.gov/pubmed/34791374
http://dx.doi.org/10.1093/molbev/msab316
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