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Development of the nervous system in Cephalocarida (Crustacea): early neuronal differentiation and successive patterning

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Abstract

The development of the nervous system in the cephalocarid Hutchinsoniella macracantha is investigated here for the first time using a combination of immunolabeling (tubulin, serotonin), nuclear counterstaining, confocal laser scanning microscopy, and computer-aided 3D reconstruction in order to compare cephalocarids to the growing number of other arthropods into which neurodevelopmental studies have been carried out. The existing description of external larval development in H. macracantha is complemented by a description of hitherto unknown embryonic and larval stages. The early embryo exhibits the three naupliar appendage anlagen (antennula, antenna, and mandible) and a short maxillular bud, all equipped with a segmental appendage nerve. As in other crustaceans, neurites of the proto-, deuto-, and tritocerebrum form a circumesophageal ring. In the late embryo, several telsonic neurons send their neurites anteriorly into the ventral nerve cord in a manner reminiscent of posterior pioneer neurons. The hatching metanauplius already comprises a well-developed brain, a subesophageal ganglion made up of three fused neuromeres, and four distinctive neuromeres containing segmental commissures in the yet limbless prospective thorax. Most postnaupliar segments arise from a distinct growth zone situated anterior to the telson that proliferates cells anteriorly. Neuronal differentiation begins before new segments are externally separated from the trunk ending and, in the thorax, before the formation of limb anlagen, i.e., earlier than in all other crustaceans studied so far. In the growth zone of one hatchling, we found a pair of large apical cells adjacent to an inward-pointing row of three smaller cells, an arrangement reminiscent of the neuroblasts and ganglion mother cells in other crustaceans. In the trunk, segmental nerves, commissures, and serotonin-like immunoreactive neurons differentiate successively from anterior to posterior. The sequence in which serially homologous neural features develop is basically the same throughout all segments of the trunk and correlated with the differentiation of limbs. It appears that the neuroanatomical differences between the adult thorax and the abdomen result from this developmental sequence stopping earlier in the abdomen than in the thorax.

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Acknowledgments

We are grateful to Georg Brenneis for his valuable spadework in immunolabeling some specimens. Thanks to George Hampson, Steve Aubrey, Christian Wirkner, Günther Jirikowski, Jonas Keiler, Bastian-Jesper Klußmann-Fricke, Martin Fritsch, and all the volunteers who helped collect cephalocarids. We thank Simone Bourgeois and the late Arthur Dutra from SeaLab, New Bedford, who kindly offered their laboratory and help during our collecting trips. We are grateful to Caterina Biffis, Steffen Harzsch, Joachim Haug, Günther Jirikowski, Carsten Wolff, and Gerhard Scholtz for their expert opinions. We appreciate the suggestions and comments of two anonymous reviewers and thank Lucy Cathrow for improving the English. Finally, we thank the German Science Foundation (DFG) for funding this project (RI 837/10-1,2) as part of the DFG priority program Deep Metazoan Phylogeny.

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  1. Allgemeine und Spezielle Zoologie, Universität Rostock, Universitätsplatz 2, 18055, Rostock, Germany

    Martin E. J. Stegner & Stefan Richter

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Communicated by Andreas Schmidt-Rhaesa.

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Stegner, M.E.J., Richter, S. Development of the nervous system in Cephalocarida (Crustacea): early neuronal differentiation and successive patterning. Zoomorphology 134, 183–209 (2015). https://doi.org/10.1007/s00435-014-0248-1

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