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      Anchored phylogenomics illuminates the skipper butterfly tree of life

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          Abstract

          Background

          Butterflies (Papilionoidea) are perhaps the most charismatic insect lineage, yet phylogenetic relationships among them remain incompletely studied and controversial. This is especially true for skippers (Hesperiidae), one of the most species-rich and poorly studied butterfly families.

          Methods

          To infer a robust phylogenomic hypothesis for Hesperiidae, we sequenced nearly 400 loci using Anchored Hybrid Enrichment and sampled all tribes and more than 120 genera of skippers. Molecular datasets were analyzed using maximum-likelihood, parsimony and coalescent multi-species phylogenetic methods.

          Results

          All analyses converged on a novel, robust phylogenetic hypothesis for skippers. Different optimality criteria and methodologies recovered almost identical phylogenetic trees with strong nodal support at nearly all nodes and all taxonomic levels. Our results support Coeliadinae as the sister group to the remaining skippers, the monotypic Euschemoninae as the sister group to all other subfamilies but Coeliadinae, and the monophyly of Eudaminae plus Pyrginae. Within Pyrginae, Celaenorrhinini and Tagiadini are sister groups, the Neotropical firetips, Pyrrhopygini, are sister to all other tribes but Celaenorrhinini and Tagiadini. Achlyodini is recovered as the sister group to Carcharodini, and Erynnini as sister group to Pyrgini. Within the grass skippers (Hesperiinae), there is strong support for the monophyly of Aeromachini plus remaining Hesperiinae. The giant skippers ( Agathymus and Megathymus) once classified as a subfamily, are recovered as monophyletic with strong support, but are deeply nested within Hesperiinae.

          Conclusions

          Anchored Hybrid Enrichment sequencing resulted in a large amount of data that built the foundation for a new, robust evolutionary tree of skippers. The newly inferred phylogenetic tree resolves long-standing systematic issues and changes our understanding of the skipper tree of life. These resultsenhance understanding of the evolution of one of the most species-rich butterfly families.

          Electronic supplementary material

          The online version of this article (10.1186/s12862-018-1216-z) contains supplementary material, which is available to authorized users.

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          Most cited references43

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          ASTRAL-II: coalescent-based species tree estimation with many hundreds of taxa and thousands of genes

          Motivation: The estimation of species phylogenies requires multiple loci, since different loci can have different trees due to incomplete lineage sorting, modeled by the multi-species coalescent model. We recently developed a coalescent-based method, ASTRAL, which is statistically consistent under the multi-species coalescent model and which is more accurate than other coalescent-based methods on the datasets we examined. ASTRAL runs in polynomial time, by constraining the search space using a set of allowed ‘bipartitions’. Despite the limitation to allowed bipartitions, ASTRAL is statistically consistent. Results: We present a new version of ASTRAL, which we call ASTRAL-II. We show that ASTRAL-II has substantial advantages over ASTRAL: it is faster, can analyze much larger datasets (up to 1000 species and 1000 genes) and has substantially better accuracy under some conditions. ASTRAL’s running time is O ( n 2 k | X | 2 ) , and ASTRAL-II’s running time is O ( n k | X | 2 ) , where n is the number of species, k is the number of loci and X is the set of allowed bipartitions for the search space. Availability and implementation: ASTRAL-II is available in open source at https://github.com/smirarab/ASTRAL and datasets used are available at http://www.cs.utexas.edu/~phylo/datasets/astral2/. Contact: smirarab@gmail.com Supplementary information: Supplementary data are available at Bioinformatics online.
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            The monarch butterfly genome yields insights into long-distance migration.

            We present the draft 273 Mb genome of the migratory monarch butterfly (Danaus plexippus) and a set of 16,866 protein-coding genes. Orthology properties suggest that the Lepidoptera are the fastest evolving insect order yet examined. Compared to the silkmoth Bombyx mori, the monarch genome shares prominent similarity in orthology content, microsynteny, and protein family sizes. The monarch genome reveals a vertebrate-like opsin whose existence in insects is widespread; a full repertoire of molecular components for the monarch circadian clockwork; all members of the juvenile hormone biosynthetic pathway whose regulation shows unexpected sexual dimorphism; additional molecular signatures of oriented flight behavior; microRNAs that are differentially expressed between summer and migratory butterflies; monarch-specific expansions of chemoreceptors potentially important for long-distance migration; and a variant of the sodium/potassium pump that underlies a valuable chemical defense mechanism. The monarch genome enhances our ability to better understand the genetic and molecular basis of long-distance migration. Copyright © 2011 Elsevier Inc. All rights reserved.
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              FASconCAT-G: extensive functions for multiple sequence alignment preparations concerning phylogenetic studies

              Background Phylogenetic and population genetic studies often deal with multiple sequence alignments that require manipulation or processing steps such as sequence concatenation, sequence renaming, sequence translation or consensus sequence generation. In recent years phylogenetic data sets have expanded from single genes to genome wide markers comprising hundreds to thousands of loci. Processing of these large phylogenomic data sets is impracticable without using automated process pipelines. Currently no stand-alone or pipeline compatible program exists that offers a broad range of manipulation and processing steps for multiple sequence alignments in a single process run. Results Here we present FASconCAT-G, a system independent editor, which offers various processing options for multiple sequence alignments. The software provides a wide range of possibilities to edit and concatenate multiple nucleotide, amino acid, and structure sequence alignment files for phylogenetic and population genetic purposes. The main options include sequence renaming, file format conversion, sequence translation between nucleotide and amino acid states, consensus generation of specific sequence blocks, sequence concatenation, model selection of amino acid replacement with ProtTest, two types of RY coding as well as site exclusions and extraction of parsimony informative sites. Convieniently, most options can be invoked in combination and performed during a single process run. Additionally, FASconCAT-G prints useful information regarding alignment characteristics and editing processes such as base compositions of single in- and outfiles, sequence areas in a concatenated supermatrix, as well as paired stem and loop regions in secondary structure sequence strings. Conclusions FASconCAT-G is a command-line driven Perl program that delivers computationally fast and user-friendly processing of multiple sequence alignments for phylogenetic and population genetic applications and is well suited for incorporation into analysis pipelines. Electronic supplementary material The online version of this article (doi:10.1186/s12983-014-0081-x) contains supplementary material, which is available to authorized users.
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                Author and article information

                Contributors
                Emmanuel.touss1@gmail.com
                Journal
                BMC Evol Biol
                BMC Evol. Biol
                BMC Evolutionary Biology
                BioMed Central (London )
                1471-2148
                19 June 2018
                19 June 2018
                2018
                : 18
                : 101
                Affiliations
                [1 ]ISNI 0000 0004 1936 8091, GRID grid.15276.37, Florida Museum of Natural History, , University of Florida, ; Gainesville, Florida, 32611 USA
                [2 ]RAPiD Genomics 747 SW 2nd Avenue IMB#14, Gainesville, FL 32601 USA
                [3 ]ISNI 0000 0001 2111 6385, GRID grid.260001.5, Evolution and Ecology Group, Department of Biology, , Middle Tennessee State University, ; Murfreesboro, TN 37132 USA
                [4 ]ISNI 0000 0001 2151 536X, GRID grid.26999.3d, The University Museum, , The University of Tokyo, ; Hongo, Bunkyo-ku, Tokyo, 113-0033 Japan
                [5 ]ISNI 0000 0001 2216 5875, GRID grid.452935.c, Arthropoda Department, Zoological Research Museum Alexander Koenig, ; Adenauer Allee 160, 53113 Bonn, Germany
                [6 ]ISNI 000000041936754X, GRID grid.38142.3c, Department of Organismic and Evolutionary Biology, , Harvard University, ; Cambridge, MA 02138 USA
                [7 ]ISNI 0000 0001 2188 3760, GRID grid.262273.0, Biology Department, City College of New York, , City University of New York, ; New York, NY 10031 USA
                [8 ]ISNI 0000 0001 2188 3760, GRID grid.262273.0, Ph.D. Program in Biology, Graduate Center, , City University of New York, ; New York, NY 10016 USA
                [9 ]Entomology Section, National Museum of the Philippines, 1000 Manila, Philippines
                Author information
                http://orcid.org/0000-0002-8439-1285
                Article
                1216
                10.1186/s12862-018-1216-z
                6011192
                29921227
                5921e102-44fc-4d37-a03d-c04a5cab62da
                © 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.

                History
                : 11 October 2017
                : 7 June 2018
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/100000001, National Science Foundation;
                Award ID: 1541557
                Categories
                Research Article
                Custom metadata
                © The Author(s) 2018

                Evolutionary Biology
                anchored hybrid enrichment,butterfly phylogenomics,coalescent multi-species,hesperiidae,lepidoptera,maximum likelihood,molecular systematics,papilionoidea,parsimony,target capture

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