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

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.

Expression of segment polarity genes in brachiopods supports a non-segmental ancestral role of engrailed for bilaterians

“…10b), suggesting that deuterostomes share a similar arrangement of gene products along the anteroposterior axis58. No nervous structures have been described at the apical/mantle boundary of larval brachiopods, so far4059. Thus, the similarity to the brachiopod pattern could indicate that such genes were also involved in the axial patterning of the last common protostome ancestor.…”

Metamorphosis in Craniiformea revisited: Novocrania anomala shows delayed development of the ventral valve

“…3D) whereas settled juveniles remain relaxed lateral muscles ( Fig. 3E and see also Altenburger and Wanninger, 2010 for a general description of the musculature in N. anomala).…”

Larval nervous systems: true larval and precocious adult

“…Phoronids and brachiopods seem to lack cerebral ganglia and are usually believed to lack the blastoporal nervous system. However, the large larva of Phoronopsis harmeri (Temereva, 2012) and the larva of the brachiopod Novocrania anomala (Altenburger and Wanninger, 2010) show paired longitudinal blastoporal nerves with a number of commissures, and this is very similar to the blastoporal nervous system of the annelids.Entoproct larvae have a paired or unpaired frontal organ/ganglion, which may be modified cerebral ganglia. The organ degenerates after metamorphosis (Nielsen, 1971).…”