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

Abstract

BackgroundDespite 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.ResultsIn 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.ConclusionsOur 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.

Never Ending Analysis of a Century Old Evolutionary Debate: “Unringing” the Urmetazoon Bell

“…Phylogenomic data sets now confirm the monophyly of Pycnogonida, Euchelicerata, Myriapoda, and Mandibulata, and within the latter clade, firmly places the Hexapoda (Insects) within the Tetraconata or Pancrustacea, a view that challenges earlier classifications that would maintain traditional boundaries among major arthropod classes, but is as yet unresolved with respect to the best supported pancrustacean sister-clade for Hexapoda (Giribet and Edgecombe, 2012;Oakley et al, 2013). Insect order-level phylogeny has seen rapid clarification of long-standing controversies over the relationships of the earliest extant insect lineages, the origin of winged insects, the relationships among the polyneopteran orders, and the origin and relationships of the holometabolan orders (Misof et al, 2014;Peters et al, 2014). While these new datasets are enormous and emphasize genetic evidence, their interpretation and analysis in the context of morphological and macroevolutionary evidence provides an example of how data combination and integration of multiple sources of evidence can flourish in a fully integrated phylogenomic research program.…”

Fleas (Siphonaptera) are Cretaceous, and evolved with Theria

“…(150-140 Mya) (Sukatsheva and Rasnitsyn, 1992), the Boreidae are thought to be at least Late Jurassic in origin, suggesting the possibility that the flea stem lineage is equally old. Recent molecular studies however have suggested that Siphonaptera and Mecoptera are sister groups (McKenna and Farrell, 2010;Misof et al, 2014;Peters et al, 2014;Wiegmann et al, 2009), Divergence time analysis on holometabolous insects with limited taxonomic representation of Siphonaptera placed the split of Mecoptera and Siphonaptera into the Triassic (Wiegmann et al, 2009) or the Jurassic , well within the age range of the recently proposed fossil ''fleas''.…”

Timeless standards for species delimitation

“…New technology-based means of gathering information have added to taxonomic quality control and sophisticated methods of data analysis. In taxonomy, new sources of data-e.g., nano CT-scan (Arillo et al 2015), evo-devo (Minelli 2015), 3D morphology (Khoury et al 2015), transcriptome phylogeny (Peters et al 2014), and cryopreservation centers-add to other sources of information and protocols that keep the biological system sound, including its nomenclature. But here again the new methods do not replace, but complement the traditional, tested methods and procedures (Schlick-Steiner et al 2010).…”