Neurogenesis in an Early Protostome Relative: Progenitor Cells in the Ventral Nerve Center of Chaetognath Hatchlings Are Arranged in a Highly Organized Geometrical Pattern

Authors

  • YVAN PEREZ,

    1. Institut Méditerranéen de Biodiversité et d'Ecologie “Evolution Genome Environment”, IMBE—UMR CNRS 7263/IRD 237 Aix-Marseille Université/Centre St Charles, Marseille cedex 3, France
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  • VERENA RIEGER,

    1. Ernst-Moritz-Arndt-Universität Greifswald, Zoologisches Institut und Museum, Cytologie und Evolutionsbiologie, Greifswald, Germany
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  • ELISE MARTIN,

    1. INSERM U845—Centre de Recherche “Croissance et Signalisation”, Hôpital Necker, Paris, France
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  • CARSTEN H.G. MÜLLER,

    1. Ernst-Moritz-Arndt-Universität Greifswald, Zoologisches Institut und Museum, Cytologie und Evolutionsbiologie, Greifswald, Germany
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  • STEFFEN HARZSCH

    Corresponding author
    • Ernst-Moritz-Arndt-Universität Greifswald, Zoologisches Institut und Museum, Cytologie und Evolutionsbiologie, Greifswald, Germany
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Correspondence to: Steffen Harzsch, Ernst-Moritz-Arndt-Universität Greifswald, Zoologisches Institut und Museum, Cytologie und Evolutionsbiologie, Johann Sebastian Bach Str. 11/12, 17497 Greifswald, Germany.

E-mail: steffen.harzsch@uni-greifswald.de

Abstract

Emerging evidence suggests that Chaetognatha represent an evolutionary lineage that is the sister group to all other Protostomia thus promoting these animals as a pivotal model for our understanding of bilaterian evolutionary history. We have analyzed the proliferation of neuronal progenitor cells in the developing ventral nerve center (VNC) of Spadella cephaloptera hatchlings. To that end, for the first time in Chaetognatha, we performed in vivo incorporation experiments with the S-phase specific mitosis marker bromodeoxyuridine (BrdU). Our experiments provide evidence for a high level of mitotic activity in the VNC for ca. 3 days after hatching. Neurogenesis is carried by presumptive neuronal progenitor cells that cycle rapidly and most likely divide asymmetrically. These progenitors are arranged in a distinct grid-like geometrical pattern including about 35 transverse rows. Considering Chaetognaths to be an early offshoot of the protostome lineage we conclude that the presence of neuronal progenitor cells with asymmetric division seems to be a feature that is rooted deeply in the Metazoa. In the light of previous evidence indicating the presence of serially iterated peptidergic neurons with individual identities in the chaetognath VNC, we discuss if these neuronal progenitor cells give rise to distinct lineages. Furthermore, we evaluate the serially iterated arrangement of the progenitor cells in the light of evolution of segmentation. J. Exp. Zool. (Mol. Dev. Evol.) 320B: 179–193, 2013. © 2013 Wiley Periodicals, Inc.

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