Neuromuscular development and metamorphosis in the serpulid polychaete Hydroides elegans

Abstract

Larvae of the serpulid polychaete Hydroides elegans display a complex range of behaviors that culminates in settlement from the water column and the induction of metamorphosis. The central nervous system of the larvae coordinates and controls these processes. Little is known about the morphology and early development of the central nervous system in polychaete larvae. Confocal laser scanning microscopy and antibodies raised against serotonin, FMRF-amide, tyrosine hydroxylase and β-tubulin were used to track neurogenesis and neural development from early in larval development through the attainment of metamorphic competence in H. elegans. It was determined that the earliest neuron was posteriorly positioned in the hyposphere and its axons may serve as a scaffolding for the later developing ventral nerve cords. Because competent larvae of H. elegans have a well developed serotonergic nervous system that innervates both the cerebral ganglia and larval structures fated to be lost during metamorphosis, seven different compounds involved in both the biosynthesis of 5-HT and those altering 5-HT signaling pathways to were tested determine if release of 5-HT coordinates and controls metamorphosis of H. elegans. Metamorphic assays utilizing these compounds demonstrated that serotonin was required for metamorphosis of H. elegans. Finally, confocal laser scanning microscopy was used to examine myogenesis in larvae of H. elegans and then to track the fate of these muscle groups through metamorphosis. Muscles associated with the larval gut and the trochal bands were the earliest muscles to develop. At competence, main muscle systems consisted of three bands of muscle associated with the trochal bands, an additional band of muscle in the episphere, two pairs of longitudinal muscles, an extensive set of muscles associated with the chaetal sacs, and a complex set of muscles surrounding the gut. The majority of these muscles persist through metamorphosis and only the ring muscles associated with the trochal bands disappear during metamorphosis. The relatively small loss of muscle and the precocious development of adult muscles during larval development and may be an evolutionary advantage that allows for the rapid metamorphosis after brief contact with a metamorphic cue.