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      The Evolution and Development of Cephalopod Chambers and Their Shape

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          Abstract

          The Ammonoidea is a group of extinct cephalopods ideal to study evolution through deep time. The evolution of the planispiral shell and complexly folded septa in ammonoids has been thought to have increased the functional surface area of the chambers permitting enhanced metabolic functions such as: chamber emptying, rate of mineralization and increased growth rates throughout ontogeny. Using nano-computed tomography and synchrotron radiation based micro-computed tomography, we present the first study of ontogenetic changes in surface area to volume ratios in the phragmocone chambers of several phylogenetically distant ammonoids and extant cephalopods. Contrary to the initial hypothesis, ammonoids do not possess a persistently high relative chamber surface area. Instead, the functional surface area of the chambers is higher in earliest ontogeny when compared to Spirula spirula. The higher the functional surface area the quicker the potential emptying rate of the chamber; quicker chamber emptying rates would theoretically permit faster growth. This is supported by the persistently higher siphuncular surface area to chamber volume ratio we collected for the ammonite Amauroceras sp. compared to either S. spirula or nautilids. We demonstrate that the curvature of the surface of the chamber increases with greater septal complexity increasing the potential refilling rates. We further show a unique relationship between ammonoid chamber shape and size that does not exist in S. spirula or nautilids. This view of chamber function also has implications for the evolution of the internal shell of coleoids, relating this event to the decoupling of soft-body growth and shell growth.

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          Cephalopod origin and evolution: A congruent picture emerging from fossils, development and molecules: Extant cephalopods are younger than previously realised and were under major selection to become agile, shell-less predators.

          Cephalopods are extraordinary molluscs equipped with vertebrate-like intelligence and a unique buoyancy system for locomotion. A growing body of evidence from the fossil record, embryology and Bayesian molecular divergence estimations provides a comprehensive picture of their origins and evolution. Cephalopods evolved during the Cambrian (∼530 Ma) from a monoplacophoran-like mollusc in which the conical, external shell was modified into a chambered buoyancy apparatus. During the mid-Palaeozoic (∼416 Ma) cephalopods diverged into nautiloids and the presently dominant coleoids. Coleoids (i.e. squids, cuttlefish and octopods) internalised their shells and, in the late Palaeozoic (∼276 Ma), diverged into Vampyropoda and the Decabrachia. This shell internalisation appears to be a unique evolutionary event. In contrast, the loss of a mineralised shell has occurred several times in distinct coleoid lineages. The general tendency of shell reduction reflects a trend towards active modes of life and much more complex behaviour. Copyright © 2011 WILEY Periodicals, Inc.
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            Allometry and size in ontogeny and phylogeny.

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              Cephalopod Hox genes and the origin of morphological novelties.

              Cephalopods are a diverse group of highly derived molluscs, including nautiluses, squids, octopuses and cuttlefish. Evolution of the cephalopod body plan from a monoplacophoran-like ancestor entailed the origin of several key morphological innovations contributing to their impressive evolutionary success. Recruitment of regulatory genes, or even pre-existing regulatory networks, may be a common genetic mechanism for generating new structures. Hox genes encode a family of transcriptional regulatory proteins with a highly conserved role in axial patterning in bilaterians; however, examples highlighting the importance of Hox gene recruitment for new developmental functions are also known. Here we examined developmental expression patterns for eight out of nine Hox genes in the Hawaiian bobtail squid Euprymna scolopes, by whole-mount in situ hybridization. Our data show that Hox orthologues have been recruited multiple times and in many ways in the origin of new cephalopod structures. The manner in which these genes have been co-opted during cephalopod evolution provides insight to the nature of the molecular mechanisms driving morphological change in the Lophotrochozoa, a clade exhibiting the greatest diversity of body plans in the Metazoa.
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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
                10 March 2016
                2016
                : 11
                : 3
                : e0151404
                Affiliations
                [1 ]Institute of Geology, Mineralogy, and Geophysics, Ruhr-Universität Bochum, Bochum, Germany
                [2 ]Museum für Naturkunde Berlin, Leibniz-Institut für Evolutions- und Biodiversitätsforschung, Berlin, Germany
                [3 ]Department of Scientific Visualization and Data Analysis, Zuse Institute, Berlin, Germany
                [4 ]Helmholtz-Zentrum Potsdam, Deutsches GeoForschungsZentrum, Potsdam, Germany
                University of California, UNITED STATES
                Author notes

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

                Conceived and designed the experiments: RL RH. Performed the experiments: RL. Analyzed the data: RL DK RH. Contributed reagents/materials/analysis tools: DK SZ ER. Wrote the paper: RL.

                Article
                PONE-D-15-54501
                10.1371/journal.pone.0151404
                4786199
                26963712
                0cc9cbb6-a050-4945-994a-63b54a7be6ca
                © 2016 Lemanis 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
                : 16 December 2015
                : 26 February 2016
                Page count
                Figures: 6, Tables: 1, Pages: 21
                Funding
                This work was supported by the Deutsche Forschungsgemeinschaft (DFG) Grant: HO 4674/2-1 to RH ( http://www.dfg.de/). The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Developmental Biology
                Morphogenesis
                Biology and Life Sciences
                Organisms
                Animals
                Invertebrates
                Molluscs
                Cephalopods
                Physical Sciences
                Physics
                Condensed Matter Physics
                Buoyancy
                Biology and Life Sciences
                Zoology
                Malacology
                Biology and Life Sciences
                Evolutionary Biology
                Organismal Evolution
                Animal Evolution
                Earth Sciences
                Geology
                Geologic Time
                Mesozoic Era
                Jurassic Period
                Biology and Life Sciences
                Evolutionary Biology
                Evolutionary Physiology
                Physical Sciences
                Physics
                Classical Mechanics
                Continuum Mechanics
                Fluid Mechanics
                Fluid Dynamics
                Custom metadata
                All relevant data are within the paper and its Supporting Information files.

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