Neural architecture of Galathowenia oculata Zach, 1923 (Oweniidae, Annelida)

Abstract

BackgroundOweniids are marine tubeworms burrowing in muddy sediments that in current phylogenies form an early branching lineage within Annelida. Little is known about their general morphology, in particular the nervous system. Here we provide an immunocytochemical investigation of the nervous system of Galathowenia oculata in order to discuss putative ancestral neuronal features in Oweniidae.ResultsAdult Galathowenia oculata have neither a supraesophageal ganglion nor ganglia associated with the ventral nerve cord. Instead, there is a dorsal brain commissure in the head collar that is engulfed by a cellular cortex. Accordingly, we herein term this neural structure “medullary brain commissure”. The anterior margin of the head collar exhibits numerous neurites that emerge from the brain commissure. The dorsolateral folds are innervated by the ventrolateral neurite bundles extending from the circumesophageal connectives. In the anterior uniramous and biramous segments immunoreactive somata are distributed evenly along the ventral nerve cord and arranged metamerically in the posterior-most short segments. One dorsal and two pairs of lateral neurite bundles extend longitudinally along the body. Numerous serially arranged circular neurite bundles were labeled in anteriormost long segments. Metameric arrangement of the circular neurite bundles stained against FMRFamide and acetylated α-tubulin is revealed in posterior short segments. For the first time immunoreactive somata arranged in clusters are reported within the pygidium in oweniids.ConclusionsDue to the lack of head appendages and a sedentary mode of life, G. oculata exhibits a single dorsal commissure (versus a brain with four commissures in most annelids). A “medullary brain commissure” is known so far only in Oweniidae and Echiura. Lack of ganglia and metamery in the ventral nerve cord of the anteriormost segments might be the result of the elongation of these segments. In the short posterior segments the metamery of immunoreactive somata and circular neurite bundles is conserved. We hypothesize that the unpaired ventral nerve cord in adult oweniids might be a result of an initially paired ventral nerve cord that fuses during development, a condition not uncommon within Annelida.

Breaking the ladder: Evolution of the ventral nerve cord in Annelida

“…In the following we refer to Richter et al [62] regarding the terminology of However, developmental studies in Owenia fusiformis reveal seriality of repeated 5-HT-LIR somata (figure 2d) [38] and investigations in adult Galathowenia oculata exhibit posterior somata clusters showing selective immunoreactivity [37]. Nevertheless, the latter results are not in contrast to the herein presented observations; they, illustrate the developmental complexity on the one hand, but also the necessity of a multimethodological approach on the other hand, as well as the importance of future analyses of larval and juvenile stages in Oweniidae.…”

“…Comparative neuroanatomical investigations focussing on these non-pleistoannelid taxa are still limited [34][35][36][37][38]. Moreover, several groups that were so far difficult to place in the annelid tree but were sometimes also considered as possibly early-branching, namely Apistobranchidae and Psammodrilidae, were neither included into recent phylogenomic studies [39,40] nor examined in detail concerning their neuroanatomy [41,42].…”

High diversity in neuropeptide immunoreactivity patterns among three closely related species of Dinophilidae (Annelida)

“…Studies on the annelid brain and major nerves conducted by serial sectioning and TEM‐studies go back several decades (Windoffer & Westheide, ; Purschke, ; Orrhage & Müller, ). The advancements in immunocytochemistry in combination with CLSM facilitated new neural descriptions in a broad range of invertebrates and has proven especially well‐suited for studies on microscopic representatives (e.g., meiofaunal taxa or temporary meiofauna such as embryos, larvae and juveniles of macroscopic species), where not only the nervous system but also its intricate relation to musculature and ciliated structures can be exposed (e.g., Hay‐Schmidt, ; Müller & Sterrer, ; Wanninger, Koop, Bromham, Noonan, & Degnan, ; McDougall, Chen, Shimeld, & Ferrier, ; Worsaae & Rouse, ; Nielsen & Worsaae, ; Worsaae & Rouse, ; Schwaha & Wanninger, ; Worsaae, Sterrer, Kaul‐Strehlow, Hay‐Schmidt, & Giribet, ; Kerbl, Bekkouche, Sterrer, & Worsaae, ; Schmidt‐Rhaesa, Harzsch, & Purschke, ; Bekkouche & Worsaae, ; ; Rimskaya‐Korsakova, Kristof, Malakhov, & Wanninger, ; Worsaae, Rimskaya‐Korsakova, & Rouse, ; Kerbl, Fofanova, Mayorova, Voronezhskaya, & Worsaae, ; Gasiorowski, Bekkouche, & Worsaae, ; Henne, Friedrich, Hammel, Sombke, & Schmidt‐Rhaesa, ; Henne, Sombke, & Schmidt‐Rhaesa, 2007b). Yet, few studies have taken advantage of the small‐sized meiofauna for studying the distribution of the numerous and proposedly highly conserved neuropeptides in adult nervous systems, using immunocytochemistry to identify putative morphological or functional regionalizations in their small and compact brain and nervous system.…”

Annelid brain and nerve cord in siboglinidRiftia pachyptila

“…Lack of ganglia in medullary nerve cord in long vestimentum/forepart and trunk segments of vestimentiferans and frenulates, and their presence in each segment of mobile frenulate opisthosome is unusual for the most annelids exhibiting the uniform structure of the nerve cord along worm body as eighter medullar, or ganglionated one [47,60,70,71]. Non-uniform ventral nerve cord is known in oweniids: nerve cord exchibits medullary state in elongated anterior segments and ganglionated-like state in short posterior segments [44,52,73]. We assume in siboglinids medullary state of nerve cords in elongated segments is due to regular innervation of the structures in the segments which is convergent to the state of oweniid nerve cord.…”