Confocal analysis of nervous system architecture in direct-developing juveniles of Neanthes arenaceodentata (Annelida, Nereididae)

Abstract

BackgroundMembers of Family Nereididae have complex neural morphology exemplary of errant polychaetes and are leading research models in the investigation of annelid nervous systems. However, few studies focus on the development of their nervous system morphology. Such data are particularly relevant today, as nereidids are the subjects of a growing body of "evo-devo" work concerning bilaterian nervous systems, and detailed knowledge of their developing neuroanatomy facilitates the interpretation of gene expression analyses. In addition, new data are needed to resolve discrepancies between classic studies of nereidid neuroanatomy. We present a neuroanatomical overview based on acetylated α-tubulin labeling and confocal microscopy for post-embryonic stages of Neanthes arenaceodentata, a direct-developing nereidid.ResultsAt hatching (2-3 chaetigers), the nervous system has developed much of the complexity of the adult (large brain, circumesophageal connectives, nerve cords, segmental nerves), and the stomatogastric nervous system is partially formed. By the 5-chaetiger stage, the cephalic appendages and anal cirri are well innervated and have clear connections to the central nervous system. Within one week of hatching (9-chaetigers), cephalic sensory structures (e.g., nuchal organs, Langdon's organs) and brain substructures (e.g., corpora pedunculata, stomatogastric ganglia) are clearly differentiated. Additionally, the segmental-nerve architecture (including interconnections) matches descriptions of other, adult nereidids, and the pharynx has developed longitudinal nerves, nerve rings, and ganglia. All central roots of the stomatogastric nervous system are distinguishable in 12-chaetiger juveniles. Evidence was also found for two previously undescribed peripheral nerve interconnections and aspects of parapodial muscle innervation.ConclusionsN. arenaceodentata has apparently lost all essential trochophore characteristics typical of nereidids. Relative to the polychaete Capitella, brain separation from a distinct epidermis occurs later in N. arenaceodentata, indicating different mechanisms of prostomial development. Our observations of parapodial innervation and the absence of lateral nerves in N. arenaceodentata are similar to a 19th century study of Alitta virens (formerly Nereis/Neanthes virens) but contrast with a more recent study that describes a single parapodial nerve pattern and lateral nerve presence in A. virens and two other genera. The latter study apparently does not account for among-nereidid variation in these major neural features.

An immunocytochemical window into the development of Platynereis massiliensis (Annelida, Nereididae)

“…In general the development of P. massiliensis is comparable to that of other errant annelids with lecithotrophic development stages, e.g., Neanthes arenaceodentata (Winchell et al, 2010) or Mooreonuphis stigmatis (Budaeva and Fauchald, 2010). All three species bear late feeding, not free-swimming juveniles with reduced ciliary bands, a large amount of yolk, and the presence of three chaetigers in early stages.…”

“…After development of adult eyes the larval eyes disappear (Arendt et al, 2002;Fischer et al, 2010). Because there are no remnants of single larval eyes and related 22C10-positive cells detectable in P. massiliensis, the loss of these structures has to be assumed.In general the development of P. massiliensis is comparable to that of other errant annelids with lecithotrophic development stages, e.g., Neanthes arenaceodentata (Winchell et al, 2010) or Mooreonuphis stigmatis (Budaeva and Fauchald, 2010). All three species bear late feeding, not free-swimming juveniles with reduced ciliary bands, a large amount of yolk, and the presence of three chaetigers in early stages.…”

“…As P. massiliensis develops without a metamorphosis, we will refer to developing stages as either embryonic or juveniles, but avoid the term larvae (see also Nielsen, 2009;Winchell et al, 2010). However, the definition of the term "larva" remains debated and alternative terminologies exist (e.g., McEdward and Janies, 1993;Pechenik, 1999).…”

“…In contrast, transitional larval characters present in P. dumerilii seem to be lost in P. massiliensis (e.g., apical organ, larval eyes). Future studies focusing of the underlying expression patterns of genes involved in the timing of the formation of these characters will help to understand the genetic mechanisms underlying heterochrony (see also Smith, 2003;Winchell et al, 2010). Besides genes traditionally targeted in evolutionary developmental studies, microRNAs might be particularly important to understand the genetic bases of heterochronic shifts (Moss, 2007).…”

Molecular phylogenetics of the Neanthes acuminata (Annelida: Nereididae) species complex

“…Los Angeles Harbour Reish, 1956 [as N. caudata], Crippen andReish, 1967, Reish, 1972 Venice, California : Winchell, et al 2010. Alamitos Bay: Reish, 1964Reish, [as N. caudata], 1972 San Gabriel River, Reish, 1972, Oshida, et al 1976. Newport Bay: Reish, 1972 Punta Banda, Mexico: Díaz-Castañeda and Rodréguez-Villanueva, 1998…”