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      Phylogeny of Dictyoptera: Dating the Origin of Cockroaches, Praying Mantises and Termites with Molecular Data and Controlled Fossil Evidence

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          Abstract

          Understanding the origin and diversification of organisms requires a good phylogenetic estimate of their age and diversification rates. This estimate can be difficult to obtain when samples are limited and fossil records are disputed, as in Dictyoptera. To choose among competing hypotheses of origin for dictyopteran suborders, we root a phylogenetic analysis (~800 taxa, 10 kbp) within a large selection of outgroups and calibrate datings with fossils attributed to lineages with clear synapomorphies. We find the following topology: (mantises, (other cockroaches, (Cryptocercidae, termites)). Our datings suggest that crown-Dictyoptera—and stem-mantises—would date back to the Late Carboniferous (~ 300 Mya), a result compatible with the oldest putative fossil of stem-dictyoptera. Crown-mantises, however, would be much more recent (~ 200 Mya; Triassic/Jurassic boundary). This pattern (i.e., old origin and more recent diversification) suggests a scenario of replacement in carnivory among polyneopterous insects. The most recent common ancestor of (cockroaches + termites) would date back to the Permian (~275 Mya), which contradicts the hypothesis of a Devonian origin of cockroaches. Stem-termites would date back to the Triassic/Jurassic boundary, which refutes a Triassic origin. We suggest directions in extant and extinct species sampling to sharpen this chronological framework and dictyopteran evolutionary studies.

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          Most cited references 44

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          Accounting for calibration uncertainty in phylogenetic estimation of evolutionary divergence times.

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            Estimating absolute rates of molecular evolution and divergence times: a penalized likelihood approach.

             J. Sanderson (2001)
            Rates of molecular evolution vary widely between lineages, but quantification of how rates change has proven difficult. Recently proposed estimation procedures have mainly adopted highly parametric approaches that model rate evolution explicitly. In this study, a semiparametric smoothing method is developed using penalized likelihood. A saturated model in which every lineage has a separate rate is combined with a roughness penalty that discourages rates from varying too much across a phylogeny. A data-driven cross-validation criterion is then used to determine an optimal level of smoothing. This criterion is based on an estimate of the average prediction error associated with pruning lineages from the tree. The methods are applied to three data sets of six genes across a sample of land plants. Optimally smoothed estimates of absolute rates entailed 2- to 10-fold variation across lineages.
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              Phylogeny of the ants: diversification in the age of angiosperms.

               C. Moreau (2006)
              We present a large-scale molecular phylogeny of the ants (Hymenoptera: Formicidae), based on 4.5 kilobases of sequence data from six gene regions extracted from 139 of the 288 described extant genera, representing 19 of the 20 subfamilies. All but two subfamilies are recovered as monophyletic. Divergence time estimates calibrated by minimum age constraints from 43 fossils indicate that most of the subfamilies representing extant ants arose much earlier than previously proposed but only began to diversify during the Late Cretaceous to Early Eocene. This period also witnessed the rise of angiosperms and most herbivorous insects.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                22 July 2015
                2015
                : 10
                : 7
                Affiliations
                [1 ]Institut de Systématique, Evolution, Biodiversité, ISYEB—UMR 7205 MNHN, CNRS, UPMC, EPHE, Sorbonne Universités, Muséum national d’Histoire naturelle, Département Systématique et Evolution, Paris, France
                [2 ]Department of Invertebrate Zoology, Cleveland Museum of Natural History, Cleveland, Ohio, United States of America
                Laboratoire Arago, FRANCE
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: FL AN PG. Performed the experiments: FL AN GJS. Analyzed the data: FL AN GJS TR RP PG. Wrote the paper: FL AN GJS TR RP PG.

                Article
                PONE-D-15-07817
                10.1371/journal.pone.0130127
                4511787
                26200914

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited

                Page count
                Figures: 9, Tables: 1, Pages: 27
                Product
                Funding
                This study was supported by Agence Nationale de la Recherche under the grant BIONEOCAL to PG ( www.agence-nationale-recherche.fr) and by the US National Science Foundation under the grant DEB-1216309 to GJS ( www.nsf.gov/funding). Any opinions, findings, and conclusions or recommendations expressed in this material are those of the authors and do not necessarily reflect the views of the National Science Foundation. Molecular analyses were partially funded by Muséum national d'Histoire naturelle ( www.mnhn.fr) under the grant “ATM – Taxonomie moléculaire: DNA barcode et gestion durable des collections” to FL. Some specimens were collected through fieldworks supported by Muséum national d'Histoire naturelle under the grant “ATM – Biodiversité actuelle et fossile. Crises, stress, restaurations et panchronisme: le message systématique” to FL.
                Categories
                Research Article
                Custom metadata
                Molecular data are held in the public database GenBank under the Accession Numbers KP986236-KP986445.

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