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      A new sensory organ in “primitive” molluscs (Polyplacophora: Lepidopleurida), and its context in the nervous system of chitons

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          Abstract

          Introduction

          Chitons (Polyplacophora) are molluscs considered to have a simple nervous system without cephalisation. The position of the class within Mollusca is the topic of extensive debate and neuroanatomical characters can provide new sources of phylogenetic data as well as insights into the fundamental biology of the organisms. We report a new discrete anterior sensory structure in chitons, occurring throughout Lepidopleurida, the order of living chitons that retains plesiomorphic characteristics.

          Results

          The novel “Schwabe organ” is clearly visible on living animals as a pair of streaks of brown or purplish pigment on the roof of the pallial cavity, lateral to or partly covered by the mouth lappets. We describe the histology and ultrastructure of the anterior nervous system, including the Schwabe organ, in two lepidopleuran chitons using light and electron microscopy. The oesophageal nerve ring is greatly enlarged and displays ganglionic structure, with the neuropil surrounded by neural somata. The Schwabe organ is innervated by the lateral nerve cord, and dense bundles of nerve fibres running through the Schwabe organ epithelium are frequently surrounded by the pigment granules which characterise the organ. Basal cells projecting to the epithelial surface and cells bearing a large number of ciliary structures may be indicative of sensory function. The Schwabe organ is present in all genera within Lepidopleurida (and absent throughout Chitonida) and represents a novel anatomical synapomorphy of the clade.

          Conclusions

          The Schwabe organ is a pigmented sensory organ, found on the ventral surface of deep-sea and shallow water chitons; although its anatomy is well understood, its function remains unknown. The anterior commissure of the chiton oesophagial nerve ring can be considered a brain. Our thorough review of the chiton central nervous system, and particularly the sensory organs of the pallial cavity, provides a context to interpret neuroanatomical homology and assess this new sense organ.

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          Most cited references22

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          Embedding in epoxy resins for ultrathin sectioning in electron microscopy.

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            Resolving the evolutionary relationships of molluscs with phylogenomic tools.

            Molluscs (snails, octopuses, clams and their relatives) have a great disparity of body plans and, among the animals, only arthropods surpass them in species number. This diversity has made Mollusca one of the best-studied groups of animals, yet their evolutionary relationships remain poorly resolved. Open questions have important implications for the origin of Mollusca and for morphological evolution within the group. These questions include whether the shell-less, vermiform aplacophoran molluscs diverged before the origin of the shelled molluscs (Conchifera) or lost their shells secondarily. Monoplacophorans were not included in molecular studies until recently, when it was proposed that they constitute a clade named Serialia together with Polyplacophora (chitons), reflecting the serial repetition of body organs in both groups. Attempts to understand the early evolution of molluscs become even more complex when considering the large diversity of Cambrian fossils. These can have multiple dorsal shell plates and sclerites or can be shell-less but with a typical molluscan radula and serially repeated gills. To better resolve the relationships among molluscs, we generated transcriptome data for 15 species that, in combination with existing data, represent for the first time all major molluscan groups. We analysed multiple data sets containing up to 216,402 sites and 1,185 gene regions using multiple models and methods. Our results support the clade Aculifera, containing the three molluscan groups with spicules but without true shells, and they support the monophyly of Conchifera. Monoplacophora is not the sister group to other Conchifera but to Cephalopoda. Strong support is found for a clade that comprises Scaphopoda (tusk shells), Gastropoda and Bivalvia, with most analyses placing Scaphopoda and Gastropoda as sister groups. This well-resolved tree will constitute a framework for further studies of mollusc evolution, development and anatomy.
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              Invertebrate neurophylogeny: suggested terms and definitions for a neuroanatomical glossary

              Background Invertebrate nervous systems are highly disparate between different taxa. This is reflected in the terminology used to describe them, which is very rich and often confusing. Even very general terms such as 'brain', 'nerve', and 'eye' have been used in various ways in the different animal groups, but no consensus on the exact meaning exists. This impedes our understanding of the architecture of the invertebrate nervous system in general and of evolutionary transformations of nervous system characters between different taxa. Results We provide a glossary of invertebrate neuroanatomical terms with a precise and consistent terminology, taxon-independent and free of homology assumptions. This terminology is intended to form a basis for new morphological descriptions. A total of 47 terms are defined. Each entry consists of a definition, discouraged terms, and a background/comment section. Conclusions The use of our revised neuroanatomical terminology in any new descriptions of the anatomy of invertebrate nervous systems will improve the comparability of this organ system and its substructures between the various taxa, and finally even lead to better and more robust homology hypotheses.
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                Author and article information

                Journal
                Front Zool
                Front. Zool
                Frontiers in Zoology
                BioMed Central
                1742-9994
                2014
                21 January 2014
                : 11
                : 7
                Affiliations
                [1 ]Queen’s University Belfast, Marine Laboratory, 12-13 The Strand, Portaferry, Co. Down BT22 1PF, Northern Ireland
                [2 ]Queen’s University Belfast, School of Biological Sciences, Lisburn Road, Belfast BT9 7BE, Northern Ireland
                [3 ]SNSB-Zoologische Staatssammlung München, Münchhausenstraße 21, Munich 81247, Germany
                [4 ]Ludwig-Maximilians Universität München, Biozentrum, Großhaderner Straße 2, Planegg-Martinsried 82152, Germany
                Article
                1742-9994-11-7
                10.1186/1742-9994-11-7
                3916795
                24447393
                a1a387c1-17b7-4645-96ce-ef260c289568
                Copyright © 2014 Sigwart et al.; licensee BioMed Central Ltd.

                This is an open access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 16 July 2013
                : 27 December 2013
                Categories
                Research

                Animal science & Zoology
                osphradium,sensory biology,mollusca,nervous system,cns,chiton,schwabe organ
                Animal science & Zoology
                osphradium, sensory biology, mollusca, nervous system, cns, chiton, schwabe organ

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