Capitellid connections: contributions from neuromuscular development of the maldanid polychaete Axiothella rubrocincta (Annelida)

Abstract

BackgroundNumerous phylogenetic analyses on polychaete annelids suggest a taxon Capitellida that comprises the three families Maldanidae, Arenicolidae and Capitellidae. Recent molecular studies support the position of the Echiura, traditionally ranked as a separate phylum, within the capitellids. In order to test the robustness of this molecular-based hypothesis we take a different approach using comparative analyses of nervous and muscle system development in the maldanid Axiothella rubrocincta. Employing immunocytochemistry in combination with confocal laserscanning microscopy, we broaden the database on capitellid organogenesis, thereby incorporating classical histological data in our analysis. Besides assessing possible shared features with the echiurans, we also discuss the variability of neural and muscular characters within the Capitellida.ResultsThe scaffold of the adult central nervous system, which is already established in early developmental stages of Axiothella, consists of cerebral commissures that give rise to simple circumesophageal connectives with fused ventral and dorsal roots and a single ventral neurite bundle. From the latter arise segmental neurites that innervate the peripheral bodywall. Since there is no observable regular pattern, and individual neurites are lost during ontogeny, their exact arrangement remains elusive. The pharynx is encircled by a prominent stomatogastric nerve ring, with a pair of anterior and lateral proboscis neurites directly connecting it to the central nervous system. One pair of ventral and one pair of dorsal longitudinal muscles form the earliest rudiments of the bodywall musculature in late larval stages, while a continuous layer of circular muscles is lacking throughout ontogeny.ConclusionsComparative neurodevelopmental analysis of capitellid and echiuran species reveals several common characters, including simple circumesophageal connectives, a single fused ventral nerve strand, and a stomatogastric ring nerve, that support a close relationship of both taxa, thus corroborating recent molecular phylogenetic analyses. The data on myogenesis show that four longitudinal muscle bands most likely represent an ancestral character not only for the Capitellida, but for the Annelida in general. Whether or not circular muscles are part of the annelid groundpattern remains uncertain.

Annelida

“…Phalloidin labeling coupled with confocal microscopy revealed an origin of muscular development posterior of the apical organ in the phyllodocid Phyllodoce groenlandica , with distinct transversal muscles starting to Fischer et al 2010 ). No circular musculature could be detected in developing stages of the maldanid Axiothella rubrocincta , even though they are present in adults (Brinkmann and Wanninger 2010b ). In contrast to the description for Phyllodoce , musculature of the digestive system develops before the body wall musculature in planktotrophic larvae of serpulids and sabellariids (McDougall et al 2006 ;Brinkmann and Wanninger 2010a ).…”

Canadia spinosa and the early evolution of the annelid nervous system

“…In contrast, some infaunal, sessile, tube dwelling, and parasitic taxa have lost several plesiomorphic features, reducing the brain and sensory organs and appendages, losing segmental ganglia, and reducing the ventral nerve cord to a single neurite bundle. This includes taxa in Sedentaria, such as Terebelliformia, where the transverse brain commissures are absent and palps have been lost ( 26 ), and the tube dwelling Maldanidae, where segmental ganglia are absent and there is a single ventral neurite bundle ( 35 ). The most extreme cases of reduction would be found in Echiura [where the nervous system only shows metamery early in ontogeny ( 36 )] and Sipuncula.…”

Development of the nervous system in Solenogastres (Mollusca) reveals putative ancestral spiralian features

“…In almost all spiralians investigated so far (see, for example, the works cited above), a single pair of longitudinal neurite bundles or nerve cords starts to form initially, regardless of the mode of development (direct versus indirect) and the total number of nerve cords eventually present in the adults, which may, for example, range between one and five in annelids [ 36 , 38 , 41 , 81 , 84 , 86 , 94 ]. Even some representatives that lack distinct longitudinal nerve cords as adults, such as brachiopods or phoronids, initially form a nervous system including paired longitudinal neurite bundles [ 91 , 93 , 95 ].…”