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      Bodily Complexity: Integrated Multicellular Organizations for Contraction-Based Motility

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          Abstract

          Compared to other forms of multicellularity, the animal case is unique. Animals—barring some exceptions—consist of collections of cells that are connected and integrated to such an extent that these collectives act as unitary, large free-moving entities capable of sensing macroscopic properties and events. This animal configuration is so well-known that it is often taken as a natural one that ‘must’ have evolved, given environmental conditions that make large free-moving units ‘obviously’ adaptive. Here we question the seemingly evolutionary inevitableness of animals and introduce a thesis of bodily complexity: The multicellular organization characteristic for typical animals requires the integration of a multitude of intrinsic bodily features between its sensorimotor, physiological, and developmental aspects, and the related contraction-based tissue- and cellular-level events and processes. The evolutionary road toward this bodily complexity involves, we argue, various intermediate organizational steps that accompany and support the wider transition from cilia-based to contraction/muscle-based motility, and which remain insufficiently acknowledged. Here, we stress the crucial and specific role played by muscle-based and myoepithelial tissue contraction—acting as a physical platform for organizing both the multicellular transmission of mechanical forces and multicellular signaling—as key foundation of animal motility, sensing and maintenance, and development. We illustrate and discuss these bodily features in the context of the four basal animal phyla—Porifera, Ctenophores, Placozoans, and Cnidarians—that split off before the bilaterians, a supergroup that incorporates all complex animals.

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          Most cited references 91

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          The Amphimedon queenslandica genome and the evolution of animal complexity.

          Sponges are an ancient group of animals that diverged from other metazoans over 600 million years ago. Here we present the draft genome sequence of Amphimedon queenslandica, a demosponge from the Great Barrier Reef, and show that it is remarkably similar to other animal genomes in content, structure and organization. Comparative analysis enabled by the sequencing of the sponge genome reveals genomic events linked to the origin and early evolution of animals, including the appearance, expansion and diversification of pan-metazoan transcription factor, signalling pathway and structural genes. This diverse 'toolkit' of genes correlates with critical aspects of all metazoan body plans, and comprises cell cycle control and growth, development, somatic- and germ-cell specification, cell adhesion, innate immunity and allorecognition. Notably, many of the genes associated with the emergence of animals are also implicated in cancer, which arises from defects in basic processes associated with metazoan multicellularity.
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            The genome of the choanoflagellate Monosiga brevicollis and the origin of metazoans.

            Choanoflagellates are the closest known relatives of metazoans. To discover potential molecular mechanisms underlying the evolution of metazoan multicellularity, we sequenced and analysed the genome of the unicellular choanoflagellate Monosiga brevicollis. The genome contains approximately 9,200 intron-rich genes, including a number that encode cell adhesion and signalling protein domains that are otherwise restricted to metazoans. Here we show that the physical linkages among protein domains often differ between M. brevicollis and metazoans, suggesting that abundant domain shuffling followed the separation of the choanoflagellate and metazoan lineages. The completion of the M. brevicollis genome allows us to reconstruct with increasing resolution the genomic changes that accompanied the origin of metazoans.
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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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                Author and article information

                Contributors
                Journal
                Front Physiol
                Front Physiol
                Front. Physiol.
                Frontiers in Physiology
                Frontiers Media S.A.
                1664-042X
                15 October 2019
                2019
                : 10
                Affiliations
                1IAS-Research Centre for Life, Mind & Society, Department of Logic and Philosophy of Science, University of the Basque Country , San Sebastián, Spain
                2Department of Product and Systems Design Engineering, Complex Systems and Service Design Lab, University of the Aegean , Syros, Greece
                3Department of Theoretical Philosophy, University of Groningen , Groningen, Netherlands
                Author notes

                Edited by: Matteo Mossio, UMR8590 Institut d’Histoire et de Philosophie des Sciences et des Techniques (IHPST), France

                Reviewed by: Stuart A. Newman, New York Medical College, United States; Emilio Lanna, Federal University of Bahia, Brazil; Laura Nuño De La Rosa, Complutense University of Madrid, Spain

                *Correspondence: Argyris Arnellos, argyris.arnellos@ 123456ehu.es ; arar@ 123456aegean.gr

                This article was submitted to Integrative Physiology, a section of the journal Frontiers in Physiology

                Article
                10.3389/fphys.2019.01268
                6803425
                Copyright © 2019 Arnellos and Keijzer.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                Page count
                Figures: 0, Tables: 0, Equations: 0, References: 101, Pages: 17, Words: 0
                Funding
                Funded by: Ministerio de Economía, Industria y Competitividad, Gobierno de España 10.13039/501100010198
                Categories
                Physiology
                Hypothesis and Theory

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