Expression of Serotonin in the Development of Patiriella species (Echinodermata: Asteroidea) with Different Modes of Development

Abstract

Serotonin expression was examined in the development of three species of seastars belonging to the genus Patiriella. These species represented three different modes of larval development, planktonic planktotrophic (P. regulars), planktonic lecithotrophic (P. calcar) and benthic lecithotrophic (P. exigua). Preneuronal serotonin-like immunoreactivity was detected in the ectoderm of the early gastrulae of P. regulars, and P. exigua up until the hatched brachiolarial stage. As serotonergic neurons appeared at the animal pole of the gastrulae of P. regulars, preneuronal serotonin expression was no longer evident in the ectodermal cells. These neurons were not associated with sensory-like structures such as an apical ciliary tuff. It is therefore suggested that serotonin in these neurons may be functioning as a trophic substance for their own growth and/or the development of the ciliated bands. These early serotonergic neurons also appeared to migrate to specific regions of the developing larva appearing to be the precursor neurons for the larval nervous system. Pharmacological depletion of serotonin, with the drug pchlorophenylalanine (L-PCPA), caused developmental abnormalities during gastrulation in P. regulars, P. calcar and P. exigua. These data suggested a morphogenetic role for serotonin during gastrulation. Drug treated P. exigua gastrulae also hatched prematurely, indicating a role for serotonin in the hatching process. Confocal immunofluorescence revealed ciliated serotonergic neurons in ganglia associated with the ciliated bands at the anterior and oral regions of the bipinnaria of P. regulars. Based on the disruption to feeding and swimming behaviour in P. regulars, induced by l -PCPA treatment, it is suggested that these ciliated serotonergic neurons function as sensory-like neurons in feeding and swimming behaviour. Reduction of serotonin content by L-PCPA also resulted in disruption to larval swimming in the lecithotrophic developer P. calcar.Serotonergic neurons were found in the brachiolarial arms and ciliated bands of P. regularis although immunoreactivity was absent from the adoral ciliated band of the mouth and the attachment disk. It is suggested that the absence of serotonergic neurons from the oral region reflects the changes in larval behaviour from a feeding state of the bipinnaria to the brachiolaria, which is primarily concerned with settlement behaviour. The brachiolarial arms and adhesive disk of the lecithotrophic developers, P. calcar and P. exigua contained numerous serotonergic neurons. The apical region of the serotonergic neurons of P. exigua and P. calcar contacted the exterior of the epithelium and it is suggested that these neurons function in sensing the substratum. The disruption of settlement behaviour in P. exigua by L-PCPA treatment also suggests a role for serotonin in attachment. Overall it appears that serotonin acts as a multifunctional neurochemical during different phases of development from the gastrula through to metamorphosis in Patiriella. Depletion of serotonin by l -PCPA was confirmed by reverse phase high performance liquid chromatography (rpHPLC). Irrespective of the morphological differences between the brachiolaria of the three species in this study, it appears that serotonergic neurons are conserved in like structures. A functional conservation of the role of serotonergic neurons in Patiriella is suggested.