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

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          Abstract

          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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          Most cited references43

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          Ultraconserved elements anchor thousands of genetic markers spanning multiple evolutionary timescales.

          Although massively parallel sequencing has facilitated large-scale DNA sequencing, comparisons among distantly related species rely upon small portions of the genome that are easily aligned. Methods are needed to efficiently obtain comparable DNA fragments prior to massively parallel sequencing, particularly for biologists working with non-model organisms. We introduce a new class of molecular marker, anchored by ultraconserved genomic elements (UCEs), that universally enable target enrichment and sequencing of thousands of orthologous loci across species separated by hundreds of millions of years of evolution. Our analyses here focus on use of UCE markers in Amniota because UCEs and phylogenetic relationships are well-known in some amniotes. We perform an in silico experiment to demonstrate that sequence flanking 2030 UCEs contains information sufficient to enable unambiguous recovery of the established primate phylogeny. We extend this experiment by performing an in vitro enrichment of 2386 UCE-anchored loci from nine, non-model avian species. We then use alignments of 854 of these loci to unambiguously recover the established evolutionary relationships within and among three ancient bird lineages. Because many organismal lineages have UCEs, this type of genetic marker and the analytical framework we outline can be applied across the tree of life, potentially reshaping our understanding of phylogeny at many taxonomic levels.
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            RASP (Reconstruct Ancestral State in Phylogenies): a tool for historical biogeography.

            We announce the release of Reconstruct Ancestral State in Phylogenies (RASP), a user-friendly software package for inferring historical biogeography through reconstructing ancestral geographic distributions on phylogenetic trees. RASP utilizes the widely used Statistical-Dispersal Vicariance Analysis (S-DIVA), the Dispersal-Extinction-Cladogenesis (DEC) model (Lagrange), a Statistical DEC model (S-DEC) and BayArea. It provides a graphical user interface (GUI) to specify a phylogenetic tree or set of trees and geographic distribution constraints, draws pie charts on the nodes of a phylogenetic tree to indicate levels of uncertainty, and generates high-quality exportable graphical results. RASP can run on both Windows and Mac OS X platforms. All documentation and source code for RASP is freely available at http://mnh.scu.edu.cn/soft/blog/RASP.
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              Accounting for calibration uncertainty in phylogenetic estimation of evolutionary divergence times.

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                Author and article information

                Contributors
                bonnieblaimer@gmail.com
                bradys@si.edu
                schultzt@si.edu
                lloydm@si.edu
                bfisher@calacademy.org
                psward@ucdavis.edu
                Journal
                BMC Evol Biol
                BMC Evol. Biol
                BMC Evolutionary Biology
                BioMed Central (London )
                1471-2148
                4 December 2015
                4 December 2015
                2015
                : 15
                : 271
                Affiliations
                [ ]Department of Entomology, National Museum of Natural History, Smithsonian Institution, Washington, DC 20560 USA
                [ ]Department of Entomology, California Academy of Sciences, San Francisco, CA 94118 USA
                [ ]Department of Entomology and Nematology, University of California-Davis, Davis, CA 95616 USA
                Article
                552
                10.1186/s12862-015-0552-5
                4670518
                46967951-a722-4382-b199-8b00143cc54f
                © 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.

                History
                : 8 October 2015
                : 26 November 2015
                Categories
                Research Article
                Custom metadata
                © The Author(s) 2015

                Evolutionary Biology
                ultraconserved elements,insect phylogenomics,ancient rapid radiations,formicinae,ant evolution

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