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      The evolutionary history of holometabolous insects inferred from transcriptome-based phylogeny and comprehensive morphological data


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          Despite considerable progress in systematics, a comprehensive scenario of the evolution of phenotypic characters in the mega-diverse Holometabola based on a solid phylogenetic hypothesis was still missing. We addressed this issue by de novo sequencing transcriptome libraries of representatives of all orders of holometabolan insects (13 species in total) and by using a previously published extensive morphological dataset. We tested competing phylogenetic hypotheses by analyzing various specifically designed sets of amino acid sequence data, using maximum likelihood (ML) based tree inference and Four-cluster Likelihood Mapping (FcLM). By maximum parsimony-based mapping of the morphological data on the phylogenetic relationships we traced evolutionary transformations at the phenotypic level and reconstructed the groundplan of Holometabola and of selected subgroups.


          In our analysis of the amino acid sequence data of 1,343 single-copy orthologous genes, Hymenoptera are placed as sister group to all remaining holometabolan orders, i.e., to a clade Aparaglossata, comprising two monophyletic subunits Mecopterida (Amphiesmenoptera + Antliophora) and Neuropteroidea (Neuropterida + Coleopterida). The monophyly of Coleopterida (Coleoptera and Strepsiptera) remains ambiguous in the analyses of the transcriptome data, but appears likely based on the morphological data. Highly supported relationships within Neuropterida and Antliophora are Raphidioptera + (Neuroptera + monophyletic Megaloptera), and Diptera + (Siphonaptera + Mecoptera). ML tree inference and FcLM yielded largely congruent results. However, FcLM, which was applied here for the first time to large phylogenomic supermatrices, displayed additional signal in the datasets that was not identified in the ML trees.


          Our phylogenetic results imply that an orthognathous larva belongs to the groundplan of Holometabola, with compound eyes and well-developed thoracic legs, externally feeding on plants or fungi. Ancestral larvae of Aparaglossata were prognathous, equipped with single larval eyes (stemmata), and possibly agile and predacious. Ancestral holometabolan adults likely resembled in their morphology the groundplan of adult neopteran insects. Within Aparaglossata, the adult’s flight apparatus and ovipositor underwent strong modifications. We show that the combination of well-resolved phylogenies obtained by phylogenomic analyses and well-documented extensive morphological datasets is an appropriate basis for reconstructing complex morphological transformations and for the inference of evolutionary histories.

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          Most cited references 35

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          Among-site rate variation and its impact on phylogenetic analyses.

           Ziheng Yang (1996)
          Although several decades of study have revealed the ubiquity of variation of evolutionary rates among sites, reliable methods for studying rate variation were not developed until very recently. Early methods fit theoretical distributions to the numbers of changes at sites inferred by parsimony and substantially underestimate the rate variation. Recent analyses show that failure to account for rate variation can have drastic effects, leading to biased dating of speciation events, biased estimation of the transition:transversion rate ratio, and incorrect reconstruction of phylogenies.
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            Inferring ancient divergences requires genes with strong phylogenetic signals.

            To tackle incongruence, the topological conflict between different gene trees, phylogenomic studies couple concatenation with practices such as rogue taxon removal or the use of slowly evolving genes. Phylogenomic analysis of 1,070 orthologues from 23 yeast genomes identified 1,070 distinct gene trees, which were all incongruent with the phylogeny inferred from concatenation. Incongruence severity increased for shorter internodes located deeper in the phylogeny. Notably, whereas most practices had little or negative impact on the yeast phylogeny, the use of genes or internodes with high average internode support significantly improved the robustness of inference. We obtained similar results in analyses of vertebrate and metazoan phylogenomic data sets. These results question the exclusive reliance on concatenation and associated practices, and argue that selecting genes with strong phylogenetic signals and demonstrating the absence of significant incongruence are essential for accurately reconstructing ancient divergences.
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              How many bootstrap replicates are necessary?

              Phylogenetic bootstrapping (BS) is a standard technique for inferring confidence values on phylogenetic trees that is based on reconstructing many trees from minor variations of the input data, trees called replicates. BS is used with all phylogenetic reconstruction approaches, but we focus here on one of the most popular, maximum likelihood (ML). Because ML inference is so computationally demanding, it has proved too expensive to date to assess the impact of the number of replicates used in BS on the relative accuracy of the support values. For the same reason, a rather small number (typically 100) of BS replicates are computed in real-world studies. Stamatakis et al. recently introduced a BS algorithm that is 1 to 2 orders of magnitude faster than previous techniques, while yielding qualitatively comparable support values, making an experimental study possible. In this article, we propose stopping criteria--that is, thresholds computed at runtime to determine when enough replicates have been generated--and we report on the first large-scale experimental study to assess the effect of the number of replicates on the quality of support values, including the performance of our proposed criteria. We run our tests on 17 diverse real-world DNA--single-gene as well as multi-gene--datasets, which include 125-2,554 taxa. We find that our stopping criteria typically stop computations after 100-500 replicates (although the most conservative criterion may continue for several thousand replicates) while producing support values that correlate at better than 99.5% with the reference values on the best ML trees. Significantly, we also find that the stopping criteria can recommend very different numbers of replicates for different datasets of comparable sizes. Our results are thus twofold: (i) they give the first experimental assessment of the effect of the number of BS replicates on the quality of support values returned through BS, and (ii) they validate our proposals for stopping criteria. Practitioners will no longer have to enter a guess nor worry about the quality of support values; moreover, with most counts of replicates in the 100-500 range, robust BS under ML inference becomes computationally practical for most datasets. The complete test suite is available at http://lcbb.epfl.ch/BS.tar.bz2, and BS with our stopping criteria is included in the latest release of RAxML v7.2.5, available at http://wwwkramer.in.tum.de/exelixis/software.html.

                Author and article information

                BMC Evol Biol
                BMC Evol. Biol
                BMC Evolutionary Biology
                BioMed Central
                20 March 2014
                : 14
                : 52
                [1 ]Zoologisches Forschungsmuseum Alexander Koenig, Abteilung Arthropoda, Adenauerallee 160, 53113 Bonn, Germany
                [2 ]Zoologisches Forschungsmuseum Alexander Koenig, Zentrum für Molekulare Biodiversitätsforschung (zmb), Adenauerallee 160, 53113 Bonn, Germany
                [3 ]CSIRO Ecosystem Sciences, Australian National Insect Collection, Clunies Ross Street, Acton ACT 2601, Australia
                [4 ]Rutgers University, Department of Ecology, Evolution and Natural Resources, New Brunswick, NJ 08901, USA
                [5 ]Naturhistorisches Museum Wien, 2. Zool. Abteilung, Burgring 7, 1010 Vienna, Austria
                [6 ]Department of Evolutionary Biology, University of Vienna, Althanstraße 14, 1090 Vienna, Austria
                [7 ]Institut für Spezifische Prophylaxe und Tropenmedizin, Medizinische Parasitologie, Medizinische Universität Wien (MUW), Kinderspitalgasse 15, 1090 Vienna, Austria
                [8 ]Heidelberg Institute for Theoretical Studies (HITS), Scientific Computing Group, Schloss-Wolfsbrunnenweg 35, 69118 Heidelberg, Germany
                [9 ]Karlsruher Institut für Technologie, Fakultät für Informatik, Postfach 698076128 Karlsruhe, Germany
                [10 ]Biozentrum Grindel und Zoologisches Museum Hamburg, Universität Hamburg, Martin-Luther-King-Platz 3, 20146 Hamburg, Germany
                [11 ]Entomology Group, Institut für Spezielle Zoologie und Evolutionsbiologie mit Phyletischem Museum, Friedrich-Schiller-Universität Jena, Erbertstraße. 1, 07743 Jena, Germany
                Copyright © 2014 Peters et al.; licensee BioMed Central Ltd.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. 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.

                Research Article

                Evolutionary Biology


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