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Ancient peptidergic neurons regulate ciliary swimming and settlement in Platynereis dumerilii

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Conzelmann,  M
Research Group Neurobiology of Marine Zooplankton, Max Planck Institute for Developmental Biology, Max Planck Society;

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Citation

Conzelmann, M. (2013). Ancient peptidergic neurons regulate ciliary swimming and settlement in Platynereis dumerilii. PhD Thesis, Eberhard-Karls-Universität, Tübingen, Germany.


Cite as: https://hdl.handle.net/21.11116/0000-000E-39B7-4
Abstract
Ciliated larval stages are widespread among marine invertebrates with a biphasic life cycle. Larvae have to regulate their swimming depth for optimal development and survival and to find suitable habitats for their settlement. In the present thesis I characterized the role of neuropeptides on ciliary swimming and settlement in larvae of the marine annelid Platynereis dumerilii. A set of Platynereis neuropeptides is expressed in sensory neurons that directly innervate the larval ciliary band. These neuropeptides influence two parameters of ciliary activity: ciliary beat frequency and ciliary closures. Thereby, they also regulate the swimming depth of Platynereis larvae in vertical migration assays. The Platynereis larval brain, that is predominantly organized of direct neuropeptidergic sensory-motor neurons, could therefore function as a simple depth gauge, responsible for adjusting the swimming depth in accordance to a variety of sensory environmental cues. Several of these Platynereis neuropeptides show a broad phyletic distribution. Specific antibodies for short conserved neuropeptide epitopes revealed a broad occurrence of peptidergic innervation of ciliary bands in mollusk, bryozoan and cnidarian larvae. These observations suggest a conserved role of neuropeptides in the regulation of ciliary swimming. In Platynereis, a MIP (myoinhibitory peptide) receptor-ligand pair is expressed in larval apical organ neurons. MIP-expressing cells have characteristics for chemosensory-neurosecretory neurons, regulating Platynereis larval settlement. Since orthologous peptides (Wamides) are also involved in the regulation of metamorphosis and settlement in cnidarian larvae, these data suggest that one of the ancient functions of Wamides may have been the regulation of marine life cycle transitions. Overall, the present work illustrates that the larval brain of Platynereis is predominantly composed of ancestral metazoan neuron types including cells with dual sensory-motor and chemosensory-neurosecretory function. Therefore, I propose that the Platynereis larval brain may represent a relic of an early stage of nervous system evolution.