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      Concatenated Analysis Sheds Light on Early Metazoan Evolution and Fuels a Modern “Urmetazoon” Hypothesis

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          There is no author summary for this article yet. Authors can add summaries to their articles on ScienceOpen to make them more accessible to a non-specialist audience.

          Abstract

          For more than a century, the origin of metazoan animals has been debated. One aspect of this debate has been centered on what the hypothetical “urmetazoon” bauplan might have been. The morphologically most simply organized metazoan animal, the placozoan Trichoplax adhaerens, resembles an intriguing model for one of several “urmetazoon” hypotheses: the placula hypothesis. Clear support for a basal position of Placozoa would aid in resolving several key issues of metazoan-specific inventions (including, for example, head–foot axis, symmetry, and coelom) and would determine a root for unraveling their evolution. Unfortunately, the phylogenetic relationships at the base of Metazoa have been controversial because of conflicting phylogenetic scenarios generated while addressing the question. Here, we analyze the sum of morphological evidence, the secondary structure of mitochondrial ribosomal genes, and molecular sequence data from mitochondrial and nuclear genes that amass over 9,400 phylogenetically informative characters from 24 to 73 taxa. Together with mitochondrial DNA genome structure and sequence analyses and Hox-like gene expression patterns, these data (1) provide evidence that Placozoa are basal relative to all other diploblast phyla and (2) spark a modernized “urmetazoon” hypothesis.

          Author Summary

          Following one of the basic principles in evolutionary biology that complex life forms derive from more primitive ancestors, it has long been believed that the higher animals, the Bilateria, arose from simpler (diploblastic) organisms such as the cnidarians (corals, polyps, and jellyfishes). A large number of studies, using different datasets and different methods, have tried to determine the most ancestral animal group as well as the ancestor of the higher animals. Here, we use “total evidence” analysis, which incorporates all available data (including morphology, genome, and gene expression data) and come to a surprising conclusion. The Bilateria and Cnidaria (together with the other diploblastic animals) are in fact sister groups: that is, they evolved in parallel from a very simple common ancestor. We conclude that the higher animals (Bilateria) and lower animals (diploblasts), probably separated very early, at the very beginning of metazoan animal evolution and independently evolved their complex body plans, including body axes, nervous system, sensory organs, and other characteristics. The striking similarities in several complex characters (such as the eyes) resulted from both lineages using the same basic genetic tool kit, which was already present in the common ancestor. The study identifies Placozoa as the most basal diploblast group and thus a living fossil genome that nicely demonstrates, not only that complex genetic tool kits arise before morphological complexity, but also that these kits may form similar morphological structures in parallel.

          Abstract

          Total evidence analyses reveal a surprise: Higher animals did not evolve from any known lower animal group.

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          Most cited references71

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          The general stochastic model of nucleotide substitution.

          DNA sequence evolution through nucleotide substitution may be assimilated to a stationary Markov process. The fundamental equations of the general model, with 12 independent substitution parameters, are used to obtain a formula which corrects the effect of multiple and parallel substitutions on the measure of evolutionary divergence between two homologous sequences. We show that only reversible models, with six independent parameters, allow the calculation of the substitution rates. Simulation experiments on DNA sequence evolution through nucleotide substitution call into question the effectiveness of the general model (and of any other more detailed description); nevertheless, the general model results are slightly superior to any of its particular cases.
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            The Trichoplax genome and the nature of placozoans.

            As arguably the simplest free-living animals, placozoans may represent a primitive metazoan form, yet their biology is poorly understood. Here we report the sequencing and analysis of the approximately 98 million base pair nuclear genome of the placozoan Trichoplax adhaerens. Whole-genome phylogenetic analysis suggests that placozoans belong to a 'eumetazoan' clade that includes cnidarians and bilaterians, with sponges as the earliest diverging animals. The compact genome shows conserved gene content, gene structure and synteny in relation to the human and other complex eumetazoan genomes. Despite the apparent cellular and organismal simplicity of Trichoplax, its genome encodes a rich array of transcription factor and signalling pathway genes that are typically associated with diverse cell types and developmental processes in eumetazoans, motivating further searches for cryptic cellular complexity and/or as yet unobserved life history stages.
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              The Limits of Amino Acid Sequence Data in Angiosperm Phylogenetic Reconstruction

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                Author and article information

                Contributors
                Role: Academic Editor
                Journal
                PLoS Biol
                pbio
                plbi
                plosbiol
                PLoS Biology
                Public Library of Science (San Francisco, USA )
                1544-9173
                1545-7885
                January 2009
                27 January 2009
                : 7
                : 1
                : e1000020
                Affiliations
                [1 ] ITZ, Ecology and Evolution, Tierärztliche Hochschule Hannover, Hannover, Germany
                [2 ] Department of Molecular, Cellular and Developmental Biology, Yale University, New Haven, Connecticut, United States of America
                [3 ] Sackler Institute for Comparative Genomics and Division of Invertebrate Zoology, American Museum of Natural History, New York, New York, United States of America
                Massey University, New Zealand
                Author notes
                * To whom correspondence should be addressed. E-mail: bernd.schierwater@ 123456ecolevol.de
                Article
                08-PLBI-RA-1774R4 plbi-07-01-19
                10.1371/journal.pbio.1000020
                2631068
                19175291
                76a604f5-5c55-4da9-849e-a88c4c7bc46c
                Copyright: © 2009 Schierwater et al. 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.
                History
                : 9 May 2008
                : 8 December 2008
                Page count
                Pages: 9
                Categories
                Research Article
                Evolutionary Biology
                Molecular Biology
                Custom metadata
                Schierwater B, Eitel M, Jakob W, Osigus H-J, Hadrys H, et al. (2009) Concatenated analysis sheds light on early metazoan evolution and fuels a modern “Urmetazoon” hypothesis. PLoS Biol 7(1): e1000020. doi: 10.1371/journal.pbio.1000020

                Life sciences
                Life sciences

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