Larval neurogenesis in Sabellaria alveolata reveals plasticity in polychaete neural patterning

Abstract

The investigation of neurogenesis in polychaetes not only facilitates insights into the developmental biology of this group, but also provides new data for phylogenetic analyses. This should eventually lead toward a better understanding of metazoan evolution including key issues such as the ontogenetic processes that underlie body segmentation. We here document the development of the larval nervous system in the polychaete Sabellaria alveolata using fluorescence-coupled antibodies directed against serotonin, FMRFamide, and tubulin in combination with confocal laser scanning microscopy and 3D reconstruction software. The overall pattern of neurogenesis in S. alveolata resembles the condition found in other planktonic polychaete trochophores where the larval neural body plan including a serotonergic prototroch nerve ring is directly followed by adult features of the nervous system such as circumesophageal connectives and paired ventral nerve cords. However, distinct features are also found in S. alveolata, such as the innervation of the apical organ with ring-shaped neurons, the low number of immunoreactive perikarya, and the lack of a posterior serotonergic cell. Moreover, in the larvae of S. alveolata, two distinct modes of neuronal development are expressed, viz. the simultaneous formation of the first three segmental neurons of the peripheral nervous system on the one hand versus the sequential appearance of the ventral commissures on the other. This highlights the complex mechanisms that underlie annelid body segmentation and indicates divergent developmental pathways within polychaete annelids that lead to the segmented nervous system of the adult.

Annelida

“…Such a posterior origin of serotonin-like immunoreactivity was also detected in another phyllodocid, in syllids, nereidids, and orbiniids (Orrhage and Müller 2005 ;McDougall et al 2006 ;Fischer et al 2010 ;Helm et al 2013 ). In contrast, the investigated sabellariids, spirorbids, and sipunculans show no evidence for a posterior serotonergic cell (Brinkmann and Wanninger 2008 ;Kristof et al 2008 ;Brinkmann and Wanninger 2009 ). Later, the adult nervous system starts to develop along pathways established by the earliest peripheral neurons of the larva.…”

“…However, other authors propose a separate development of the larval and adult nervous system (Lacalli 1984 ) or fi nd that the larval nervous system is integrated in the adult one (Hay-Schmidt 1995 ). The relative timing of events during neurogenesis shows major shifts between compared species and is regarded as cases of heterochrony (McDougall et al 2006 ;Brinkmann and Wanninger 2008 ;Helm et al 2013 ).…”

“…Besides this, only few comprehensive studies for developmental sequences of annelids combining immunocytochemical staining coupled with confocal laser scanning microscopy exist (Hessling 2002 ;Hessling and Westheide 2002 ;Voronezhskaya et al 2003 ;McDougall et al 2006 ;Brinkmann and Wanninger 2008 ;Kristof et al 2008 ;Fischer et al 2010 ;Winchell et al 2010 ;Helm et al 2013 , in press ). Main targets for these studies were serotonin, a biogenic amine involved in neuronal signaling, and the neuropeptide FMRFamide.…”

Sabellariidae from Lizard Island, Great Barrier Reef, including a new species of Lygdamis and notes on external morphology of the median organ

“…Members of this family show a high degree of cephalization and the nuchal nerves extend forward (i.e., to anterior end of operculum) (Orrhage 1978(Orrhage , 1980Brinkmann & Wanninger 2008). Sensory organs, such as the apical organ, palps, tentacles, statocysts, eyespots and nuchal organs have been documented in sabellariid larvae and adult stages (Orrhage 1978;Kirtley 1994).…”

Serotonergic and FMRFamidergic nervous systems in gymnolaemate bryozoan larvae

“…Two serotonergic cells are found dorsally beneath and associated with the prototroch ring nerve in Phyllodoce maculata, whereas it consists only of Wbers in Polygordius lacteus and Pomatoceros lamarckii. In Sabellaria alveolata, an apical nerve ring was found, which later fuses to form the cerebral ganglion (Brinkmann and Wanninger 2008). In Owenia fusiformis serotonergic innervation of the ciliary band as well as serotonergic neurons in the apical organ are lacking completely (Hay-Schmidt 2000).…”