Neuromuscular development in Novocrania anomala: evidence for the presence of serotonin and a spiralian-like apical organ in lecithotrophic brachiopod larvae

Evol Dev. 2010 Jan-Feb;12(1):16-24. doi: 10.1111/j.1525-142X.2009.00387.x.

Abstract

The phylogenetic position of Brachiopoda remains unsettled, and only few recent data on brachiopod organogenesis are currently available. In order to contribute data to questions concerning brachiopod ontogeny and evolution we investigated nervous and muscle system development in the craniiform (inarticulate) brachiopod Novocrania anomala. Larvae of this species are lecithotrophic and have a bilobed body with three pairs of dorsal setal bundles that emerge from the posterior lobe. Fully developed larvae exhibit a network of setae pouch muscles as well as medioventral longitudinal and transversal muscles. After settlement, the anterior and posterior adductor muscles and delicate mantle retractor muscles begin to form. Comparison of the larval muscular system of Novocrania anomala with that of rhynchonelliform (articulate) brachiopod larvae shows that the former has a much simpler muscular organization. The first signal of serotonin-like immunoreactivity appears in fully developed Novocrania anomala larvae, which have an apical organ that consists of four flask-shaped cells and two ventral neurites. These ventral neurites do not stain positively for the axonal marker alpha-tubulin in the larval stages. In the juveniles, the nervous system stained by alpha-tubulin is characterized by two ventral neurite bundles with three commissures. Our data are the first direct proof for the presence of an immunoreactive neurotransmitter in lecithotrophic brachiopod larvae and demonstrate the existence of flask-shaped serotonergic cells in the brachiopod larval apical organ, thus significantly increasing the probability that this cell type was part of the bauplan of the larvae of the last common lophotrochozoan ancestor.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Actins / metabolism
  • Animals
  • Biological Evolution
  • Imaging, Three-Dimensional
  • Immunohistochemistry
  • Invertebrates / growth & development*
  • Invertebrates / metabolism*
  • Larva / growth & development
  • Larva / metabolism
  • Microscopy, Confocal
  • Muscle Development
  • Neurogenesis
  • Phylogeny
  • Serotonin / metabolism*

Substances

  • Actins
  • Serotonin