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

Laurent Formery (1) , François Orange (2) , Antoine Formery , Shunsuke Yaguchi (3) , Christopher Lowe (4) , Michael Schubert (1) , Jenifer C. Croce (1)

1 LBDV - Laboratoire de Biologie du Développement de Villefranche sur mer
2 CCMA - Centre Commun de Microscopie Appliquée
3 Université de Tsukuba = University of Tsukuba
4 Hopkins Marine Station [Stanford]

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.

Mots clés: Comparative anatomy; evolution; juvenile; sea urchin; sea cucumber; sea star

Domaines: Embryologie et organogenèse; Zoologie des invertébrés

Laurent Formery, François Orange, Antoine Formery, Shunsuke Yaguchi, Christopher Lowe, et al.. Neural anatomy of echinoid early juveniles and comparison of nervous system organization in echinoderms. Journal of Comparative Neurology, 2021, 529, pp.1135-1156. ⟨10.1002/cne.25012⟩. ⟨hal-02929239⟩