Neurogenesis in directly and indirectly developing enteropneusts: of nets and cords

Sabrina Kaul-Strehlow, Makoto Urata, Takuya Minokawa, Thomas Stach, Andreas Wanninger

Research output: Contribution to journalArticlepeer-review

16 Citations (Scopus)

Abstract

Concerning the evolution of deuterostomes, enteropneusts (acorn worms) occupy a pivotal role as they share some characteristics with chordates (e.g., tunicates and vertebrates) but are also closely related to echinoderms (e.g., sea urchin). The nervous system in particular can be a highly informative organ system for evolutionary inferences, and advances in fluorescent microscopy have revealed overwhelming data sets on neurogenesis in various clades. However, immunocytochemical descriptions of neurogenesis of juvenile enteropneusts are particularly scarce, impeding the reconstruction of nervous system evolution in this group. We followed morphogenesis of the nervous system in two enteropneust species, one with direct (Saccoglossus kowalevskii) and the other with indirect development (Balanoglossus misakiensis), using an antibody against serotonin and electron microscopy. We found that all serotonin-like immunoreactive (LIR) neurons in both species are bipolar ciliary neurons that are intercalated between other epidermal cells. Unlike the tornaria larva of B. misakiensis, the embryonic nervous system of S. kowalevskii lacks serotonin-LIR neurons in the apical region as well as an opisthotroch neurite ring. Comparative analysis of both species shows that the projections of the serotonin-LIR somata initially form a basiepidermal plexus throughout the body that disappears within the trunk region soon after settlement before the concentrated dorsal and ventral neurite bundles emerge. Our data reveal a highly conserved mode of neurogenesis in enteropneusts that is independent of the developing mode and is inferred to be a common feature for Enteropneusta. Moreover, all detected serotonin-LIR neurons are presumably receptor cells, and the absence of serotonin-LIR interneurons from the enteropneust nervous system, which are otherwise common in various bilaterian central nervous systems, is interpreted as a loss that might have occurred already in the last common ancestor of Ambulacraria.

Original languageEnglish
Pages (from-to)405-422
Number of pages18
JournalOrganisms Diversity and Evolution
Volume15
Issue number2
DOIs
Publication statusPublished - 2015 Jun 6

Keywords

  • Bipolar receptor cell
  • Deuterostome
  • Enteropneusts
  • Evolution
  • Hemichordates
  • Nervous system
  • Neurogenesis
  • Plexus
  • Serotonin

ASJC Scopus subject areas

  • Ecology, Evolution, Behavior and Systematics

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