Volume 529, Issue 6 p. 1135-1156
RESEARCH ARTICLE

Neural anatomy of echinoid early juveniles and comparison of nervous system organization in echinoderms

Laurent Formery

Laboratoire de Biologie du Développement de Villefranche‐sur‐Mer (LBDV), Evolution of Intracellular Signaling in Development (EvoInSiDe), Sorbonne Université, CNRS, Villefranche‐sur‐Mer, France

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François Orange

Centre Commun de Microscopie Appliquée (CCMA), Université Côte d'Azur, Nice, France

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Antoine Formery

Freelance 3D Modelization, Paris, France

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Shunsuke Yaguchi

Shimoda Marine Research Center, University of Tsukuba, Shizuoka, Japan

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Christopher J. Lowe

Department of Biology, Hopkins Marine Station, Stanford University, Pacific Grove, California, USA

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Michael Schubert

Laboratoire de Biologie du Développement de Villefranche‐sur‐Mer (LBDV), Evolution of Intracellular Signaling in Development (EvoInSiDe), Sorbonne Université, CNRS, Villefranche‐sur‐Mer, France

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Jenifer C. Croce

Corresponding Author

Laboratoire de Biologie du Développement de Villefranche‐sur‐Mer (LBDV), Evolution of Intracellular Signaling in Development (EvoInSiDe), Sorbonne Université, CNRS, Villefranche‐sur‐Mer, France

Correspondence

Jenifer C. Croce, Laboratoire de Biologie du Développement de Villefranche‐sur‐Mer (LBDV), UMR7009, Institut de la Mer de Villefranche (IMEV), 181 Chemin du Lazaret, 06230 Villefranche‐sur‐Mer, France.

Email: jenifer.croce@obs-vlfr.fr

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First published: 25 August 2020

Funding information: André Picard Network; French Ministry of Research and Technology, Grant/Award Number: 2173/2015; Japan Society for the Promotion of Science, Grant/Award Number: PE18758; National Aeronautics and Space Administration, Grant/Award Number: NNX13AI68G

Abstract

The echinoderms are a phylum of marine deuterostomes characterized by the pentaradial (five fold) symmetry of their adult bodies. Due to this unusual body plan, adult echinoderms have long been excluded from comparative analyses aimed at understanding the origin and evolution of deuterostome nervous systems. Here, we investigated the neural anatomy of early juveniles of representatives of three of the five echinoderm classes: the echinoid Paracentrotus lividus, the asteroid Patiria miniata, and the holothuroid Parastichopus parvimensis. Using whole mount immunohistochemistry and confocal microscopy, we found that the nervous system of echinoid early juveniles is composed of three main structures: a basiepidermal nerve plexus, five radial nerve cords connected by a circumoral nerve ring, and peripheral nerves innervating the appendages. Our whole mount preparations further allowed us to obtain thorough descriptions of these structures and of several innervation patterns, in particular at the level of the appendages. Detailed comparisons of the echinoid juvenile nervous system with those of asteroid and holothuroid juveniles moreover supported a general conservation of the main neural structures in all three species, including at the level of the appendages. Our results support the previously proposed hypotheses for the existence of two neural units in echinoderms: one consisting of the basiepidermal nerve plexus to process sensory stimuli locally and one composed of the radial nerve cords and the peripheral nerves constituting a centralized control system. This study provides the basis for more in‐depth comparisons of the echinoderm adult nervous system with those of other animals, in particular hemichordates and chordates, to address the long‐standing controversies about deuterostome nervous system evolution.

PEER REVIEW

The peer review history for this article is available at https://publons.com/publon/10.1002/cne.25012.

DATA AVAILABILITY STATEMENT

The authors confirm that the data supporting the findings of this study are available within the article and its supplementary material.

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