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Phylogenomics of a rapid radiation: the Australian rainbow skinks

BACKGROUND: The application of target capture with next-generation sequencing now enables phylogenomic analyses of rapidly radiating clades of species. But such analyses are complicated by extensive incomplete lineage sorting, demanding the use of methods that consider this process explicitly, such...

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Autores principales: Bragg, Jason G., Potter, Sally, Afonso Silva, Ana C., Hoskin, Conrad J., Bai, Benjamin Y. H., Moritz, Craig
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5800007/
https://www.ncbi.nlm.nih.gov/pubmed/29402211
http://dx.doi.org/10.1186/s12862-018-1130-4
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author Bragg, Jason G.
Potter, Sally
Afonso Silva, Ana C.
Hoskin, Conrad J.
Bai, Benjamin Y. H.
Moritz, Craig
author_facet Bragg, Jason G.
Potter, Sally
Afonso Silva, Ana C.
Hoskin, Conrad J.
Bai, Benjamin Y. H.
Moritz, Craig
author_sort Bragg, Jason G.
collection PubMed
description BACKGROUND: The application of target capture with next-generation sequencing now enables phylogenomic analyses of rapidly radiating clades of species. But such analyses are complicated by extensive incomplete lineage sorting, demanding the use of methods that consider this process explicitly, such as the multispecies coalescent (MSC) model. However, the MSC makes strong assumptions about divergence history and population structure, and when using the full Bayesian implementation, current computational limits mean that relatively few loci and samples can be analysed for even modest sized radiations. We explore these issues through analyses of an extensive (> 1000 loci) dataset for the Australian rainbow skinks. This group consists of 3 genera and 41 described species, which likely diversified rapidly in Australia during the mid-late Miocene to occupy rainforest, woodland, and rocky habitats with corresponding diversity of morphology and breeding colouration. Previous phylogenetic analyses of this group have revealed short inter-nodes and high discordance among loci, limiting the resolution of inferred trees. A further complication is that many species have deep phylogeographic structure – this poses the question of how to sample individuals within species for analyses using the MSC. RESULTS: Phylogenies obtained using concatenation and summary coalescent species tree approaches to the full dataset are well resolved with generally consistent topology, including for previously intractable relationships near the base of the clade. As expected, branch lengths at the tips are substantially overestimated using concatenation. Comparisons of different strategies for sampling haplotypes for full Bayesian MSC analyses (for one clade and using smaller sets of loci) revealed, unexpectedly, that combining haplotypes across divergent phylogeographic lineages yielded consistent species trees. CONCLUSIONS: This study of more than 1000 loci provides a strongly-supported estimate of the phylogeny of the Australian rainbow skinks, which will inform future research on the evolution and taxonomy of this group. Our analyses suggest that species tree estimation with the MSC can be quite robust to violation of the assumption that the individuals representing a taxon are sampled from a panmictic population. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12862-018-1130-4) contains supplementary material, which is available to authorized users.
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spelling pubmed-58000072018-02-13 Phylogenomics of a rapid radiation: the Australian rainbow skinks Bragg, Jason G. Potter, Sally Afonso Silva, Ana C. Hoskin, Conrad J. Bai, Benjamin Y. H. Moritz, Craig BMC Evol Biol Research Article BACKGROUND: The application of target capture with next-generation sequencing now enables phylogenomic analyses of rapidly radiating clades of species. But such analyses are complicated by extensive incomplete lineage sorting, demanding the use of methods that consider this process explicitly, such as the multispecies coalescent (MSC) model. However, the MSC makes strong assumptions about divergence history and population structure, and when using the full Bayesian implementation, current computational limits mean that relatively few loci and samples can be analysed for even modest sized radiations. We explore these issues through analyses of an extensive (> 1000 loci) dataset for the Australian rainbow skinks. This group consists of 3 genera and 41 described species, which likely diversified rapidly in Australia during the mid-late Miocene to occupy rainforest, woodland, and rocky habitats with corresponding diversity of morphology and breeding colouration. Previous phylogenetic analyses of this group have revealed short inter-nodes and high discordance among loci, limiting the resolution of inferred trees. A further complication is that many species have deep phylogeographic structure – this poses the question of how to sample individuals within species for analyses using the MSC. RESULTS: Phylogenies obtained using concatenation and summary coalescent species tree approaches to the full dataset are well resolved with generally consistent topology, including for previously intractable relationships near the base of the clade. As expected, branch lengths at the tips are substantially overestimated using concatenation. Comparisons of different strategies for sampling haplotypes for full Bayesian MSC analyses (for one clade and using smaller sets of loci) revealed, unexpectedly, that combining haplotypes across divergent phylogeographic lineages yielded consistent species trees. CONCLUSIONS: This study of more than 1000 loci provides a strongly-supported estimate of the phylogeny of the Australian rainbow skinks, which will inform future research on the evolution and taxonomy of this group. Our analyses suggest that species tree estimation with the MSC can be quite robust to violation of the assumption that the individuals representing a taxon are sampled from a panmictic population. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12862-018-1130-4) contains supplementary material, which is available to authorized users. BioMed Central 2018-02-05 /pmc/articles/PMC5800007/ /pubmed/29402211 http://dx.doi.org/10.1186/s12862-018-1130-4 Text en © The Author(s). 2018 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Bragg, Jason G.
Potter, Sally
Afonso Silva, Ana C.
Hoskin, Conrad J.
Bai, Benjamin Y. H.
Moritz, Craig
Phylogenomics of a rapid radiation: the Australian rainbow skinks
title Phylogenomics of a rapid radiation: the Australian rainbow skinks
title_full Phylogenomics of a rapid radiation: the Australian rainbow skinks
title_fullStr Phylogenomics of a rapid radiation: the Australian rainbow skinks
title_full_unstemmed Phylogenomics of a rapid radiation: the Australian rainbow skinks
title_short Phylogenomics of a rapid radiation: the Australian rainbow skinks
title_sort phylogenomics of a rapid radiation: the australian rainbow skinks
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5800007/
https://www.ncbi.nlm.nih.gov/pubmed/29402211
http://dx.doi.org/10.1186/s12862-018-1130-4
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