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Phylogenomic methods outperform traditional multi-locus approaches in resolving deep evolutionary history: a case study of formicine ants

BACKGROUND: Ultraconserved elements (UCEs) have been successfully used in phylogenomics for a variety of taxa, but their power in phylogenetic inference has yet to be extensively compared with that of traditional Sanger sequencing data sets. Moreover, UCE data on invertebrates, including insects, ar...

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Autores principales: Blaimer, Bonnie B., Brady, Seán G., Schultz, Ted R., Lloyd, Michael W., Fisher, Brian L., Ward, Philip S.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4670518/
https://www.ncbi.nlm.nih.gov/pubmed/26637372
http://dx.doi.org/10.1186/s12862-015-0552-5
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author Blaimer, Bonnie B.
Brady, Seán G.
Schultz, Ted R.
Lloyd, Michael W.
Fisher, Brian L.
Ward, Philip S.
author_facet Blaimer, Bonnie B.
Brady, Seán G.
Schultz, Ted R.
Lloyd, Michael W.
Fisher, Brian L.
Ward, Philip S.
author_sort Blaimer, Bonnie B.
collection PubMed
description BACKGROUND: Ultraconserved elements (UCEs) have been successfully used in phylogenomics for a variety of taxa, but their power in phylogenetic inference has yet to be extensively compared with that of traditional Sanger sequencing data sets. Moreover, UCE data on invertebrates, including insects, are sparse. We compared the phylogenetic informativeness of 959 UCE loci with a multi-locus data set of ten nuclear markers obtained via Sanger sequencing, testing the ability of these two types of data to resolve and date the evolutionary history of the second most species-rich subfamily of ants in the world, the Formicinae. RESULTS: Phylogenetic analyses show that UCEs are superior in resolving ancient and shallow relationships in formicine ants, demonstrated by increased node support and a more resolved phylogeny. Phylogenetic informativeness metrics indicate a twofold improvement relative to the 10-gene data matrix generated from the identical set of taxa. We were able to significantly improve formicine classification based on our comprehensive UCE phylogeny. Our divergence age estimations, using both UCE and Sanger data, indicate that crown-group Formicinae are older (104–117 Ma) than previously suggested. Biogeographic analyses infer that the diversification of the subfamily has occurred on all continents with no particular hub of cladogenesis. CONCLUSIONS: We found UCEs to be far superior to the multi-locus data set in estimating formicine relationships. The early history of the clade remains uncertain due to ancient rapid divergence events that are unresolvable even with our genomic-scale data, although this might be largely an effect of several problematic taxa subtended by long branches. Our comparison of divergence ages from both Sanger and UCE data demonstrates the effectiveness of UCEs for dating analyses. This comparative study highlights both the promise and limitations of UCEs for insect phylogenomics, and will prove useful to the growing number of evolutionary biologists considering the transition from Sanger to next-generation sequencing approaches. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12862-015-0552-5) contains supplementary material, which is available to authorized users.
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spelling pubmed-46705182015-12-06 Phylogenomic methods outperform traditional multi-locus approaches in resolving deep evolutionary history: a case study of formicine ants Blaimer, Bonnie B. Brady, Seán G. Schultz, Ted R. Lloyd, Michael W. Fisher, Brian L. Ward, Philip S. BMC Evol Biol Research Article BACKGROUND: Ultraconserved elements (UCEs) have been successfully used in phylogenomics for a variety of taxa, but their power in phylogenetic inference has yet to be extensively compared with that of traditional Sanger sequencing data sets. Moreover, UCE data on invertebrates, including insects, are sparse. We compared the phylogenetic informativeness of 959 UCE loci with a multi-locus data set of ten nuclear markers obtained via Sanger sequencing, testing the ability of these two types of data to resolve and date the evolutionary history of the second most species-rich subfamily of ants in the world, the Formicinae. RESULTS: Phylogenetic analyses show that UCEs are superior in resolving ancient and shallow relationships in formicine ants, demonstrated by increased node support and a more resolved phylogeny. Phylogenetic informativeness metrics indicate a twofold improvement relative to the 10-gene data matrix generated from the identical set of taxa. We were able to significantly improve formicine classification based on our comprehensive UCE phylogeny. Our divergence age estimations, using both UCE and Sanger data, indicate that crown-group Formicinae are older (104–117 Ma) than previously suggested. Biogeographic analyses infer that the diversification of the subfamily has occurred on all continents with no particular hub of cladogenesis. CONCLUSIONS: We found UCEs to be far superior to the multi-locus data set in estimating formicine relationships. The early history of the clade remains uncertain due to ancient rapid divergence events that are unresolvable even with our genomic-scale data, although this might be largely an effect of several problematic taxa subtended by long branches. Our comparison of divergence ages from both Sanger and UCE data demonstrates the effectiveness of UCEs for dating analyses. This comparative study highlights both the promise and limitations of UCEs for insect phylogenomics, and will prove useful to the growing number of evolutionary biologists considering the transition from Sanger to next-generation sequencing approaches. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12862-015-0552-5) contains supplementary material, which is available to authorized users. BioMed Central 2015-12-04 /pmc/articles/PMC4670518/ /pubmed/26637372 http://dx.doi.org/10.1186/s12862-015-0552-5 Text en © Blaimer et al. 2015 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
Blaimer, Bonnie B.
Brady, Seán G.
Schultz, Ted R.
Lloyd, Michael W.
Fisher, Brian L.
Ward, Philip S.
Phylogenomic methods outperform traditional multi-locus approaches in resolving deep evolutionary history: a case study of formicine ants
title Phylogenomic methods outperform traditional multi-locus approaches in resolving deep evolutionary history: a case study of formicine ants
title_full Phylogenomic methods outperform traditional multi-locus approaches in resolving deep evolutionary history: a case study of formicine ants
title_fullStr Phylogenomic methods outperform traditional multi-locus approaches in resolving deep evolutionary history: a case study of formicine ants
title_full_unstemmed Phylogenomic methods outperform traditional multi-locus approaches in resolving deep evolutionary history: a case study of formicine ants
title_short Phylogenomic methods outperform traditional multi-locus approaches in resolving deep evolutionary history: a case study of formicine ants
title_sort phylogenomic methods outperform traditional multi-locus approaches in resolving deep evolutionary history: a case study of formicine ants
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4670518/
https://www.ncbi.nlm.nih.gov/pubmed/26637372
http://dx.doi.org/10.1186/s12862-015-0552-5
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