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Open Access Highly Accessed Research article

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

Ralph S Peters1, Karen Meusemann23, Malte Petersen2, Christoph Mayer2, Jeanne Wilbrandt2, Tanja Ziesmann2, Alexander Donath2, Karl M Kjer4, Ulrike Aspöck56, Horst Aspöck7, Andre Aberer8, Alexandros Stamatakis89, Frank Friedrich10, Frank Hünefeld11, Oliver Niehuis2, Rolf G Beutel11 and Bernhard Misof2*

Author Affiliations

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

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BMC Evolutionary Biology 2014, 14:52  doi:10.1186/1471-2148-14-52

Published: 20 March 2014

Abstract

Background

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.

Results

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.

Conclusions

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.