Research Article: The neuroanatomy of the siboglinid Riftia pachyptila highlights sedentarian annelid nervous system evolution

Date Published: December 13, 2018

Publisher: Public Library of Science

Author(s): Nadezhda N. Rimskaya-Korsakova, Sergey V. Galkin, Vladimir V. Malakhov, Andreas Hejnol.

http://doi.org/10.1371/journal.pone.0198271

Abstract

Tracing the evolution of the siboglinid group, peculiar group of marine gutless annelids, requires the detailed study of the fragmentarily explored central nervous system of vestimentiferans and other siboglinids. 3D reconstructions of the neuroanatomy of Riftia revealed that the “brain” of adult vestimentiferans is a fusion product of the supraesophageal and subesophageal ganglia. The supraesophageal ganglion-like area contains the following neural structures that are homologous to the annelid elements: the peripheral perikarya of the brain lobes, two main transverse commissures, mushroom-like structures, commissural cell cluster, and the circumesophageal connectives with two roots which give rise to the palp neurites. Three pairs of giant perikarya are located in the supraesophageal ganglion, giving rise to the paired giant axons. The circumesophageal connectives run to the VNC. The subesophageal ganglion-like area contains a tripartite ventral aggregation of perikarya (= the postoral ganglion of the VNC) interconnected by the subenteral commissure. The paired VNC is intraepidermal, not ganglionated over most of its length, associated with the ciliary field, and comprises the giant axons. The pairs of VNC and the giant axons fuse posteriorly. Within siboglinids, the vestimentiferans are distinguished by a large and considerably differentiated brain. This reflects the derived development of the tentacle crown. The tentacles of vestimentiferans are homologous to the annelid palps based on their innervation from the dorsal and ventral roots of the circumesophageal connectives. Neuroanatomy of the vestimentiferan brains is close to the brains of Cirratuliiformia and Spionida/Sabellida, which have several transverse commissures, specific position of the giant somata (if any), and palp nerve roots (if any). The palps and palp neurite roots originally developed in all main annelid clades (basally branching, errantian and sedentarian annelids), show the greatest diversity in their number in sedentarian species. Over the course of evolution of Sedentaria, the number of palps and their nerve roots either dramatically increased (as in vestimentiferan siboglinids) or were lost.

Partial Text

Vestimentifera is a peculiar group of marine gutless annelids mainly inhabiting hydrothermal vents and hydrocarbon seeps [1–3]. Vestimentiferan tubeworms, together with Frenulata [4], Sclerolinum [5] and the bone-eating worms Osedax [6], comprise the annelid group Siboglinidae [7]. The phylogenetic position of Vestimentifera and the whole group Siboglinidae in the annelid system remains controversial. Various annelid sister groups, occuping positions far from each other in the annelid tree, have been proposed, e.g. Oweniidae [8,9], Sabellidae [10,11], Cirratuliformia [12,13], or Clitellata [14,15]. The very peculiar morphology of the vestimentifera and other siboglinids is one reason why their phylogenetic position remains unresolved. Importantly, no comprehensive comparative anatomical study of the organ systems, including neural anatomy, is available to logically favor one of the hypothesized annelid affinities of siboglinids.

A comparative neuroanatomical analysis of the siboglinids and the annelid sister clades enables us to hypothesize that the last common ancestor of siboglinids had separate supra- and subesophageal ganglia, two roots of the circumesophageal connectives giving rise to neurite bundles to numerous palps, a commissural cell cluster, a paired ventral nerve cord, and had giant perikarya in the supraesophageal ganglion with paired giant axons running within the paired nerve cord (Fig 12). The strands of the VNC and the giant axons probably fused posteriorly. Notably, within Sedentaria siboglinids form the sister clade with the Cirratuliformia, and Spionida/Sabellida having the complex brain with the similar structures, like several transverse commissures and palp neurites. Siboglinids do not exhibit reduction in neuroanatomical complexity, like terebellids and pectinariids, which have no traces of commissures of the circumesophageal roots as well as no palp neurites. Future neuroanatomical studies should reveal if within the Sedentaria the simplification of the brain was the one of the trends of their evolution.

 

Source:

http://doi.org/10.1371/journal.pone.0198271

 

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