Neural reconstruction of bone-eating Osedax spp. (Annelida) and evolution of the siboglinid nervous system

Abstract

BackgroundBone-devouring Osedax worms were described over a decade ago from deep-sea whale falls. The gutless females (and in one species also the males) have a unique root system that penetrates the bone and nourishes them via endosymbiotic bacteria. Emerging from the bone is a cylindrical trunk, which is enclosed in a transparent tube, that generally gives rise to a plume of four palps (or tentacles). In most Osedax species, dwarf males gather in harems along the female’s trunk and the nervous system of these microscopic forms has been described in detail. Here, the nervous system of bone-eating Osedax forms are described for the first time, allowing for hypotheses on how the abberant ventral brain and nervous system of Siboglinidae may have evolved from a ganglionated nervous system with a dorsal brain, as seen in most extant annelids.ResultsThe intraepidermal nervous systems of four female Osedax spp. and the bone-eating O. priapus male were reconstructed in detail by a combination of immunocytochemistry, CLSM, histology and TEM. They all showed a simple nervous system composed of an anterior ventral brain, connected with anteriorly directed paired palp and gonoduct nerves, and four main pairs of posteriorly directed longitudinal nerves (2 ventral, 2 ventrolateral, 2 sets of dorso-lateral, 2 dorsal). Transverse peripheral nerves surround the trunk, ovisac and root system. The nervous system of Osedax resembles that of other siboglinids, though possibly presenting additional lateral and dorsal longitudinal nerves. It differs from most Sedentaria in the presence of an intraepidermal ventral brain, rather than a subepidermal dorsal brain, and by having an intraepidermal nerve cord with several plexi and up to three main commissures along the elongated trunk, which may comprise two indistinct segments.ConclusionsOsedax shows closer neuroarchitectural resemblance to Vestimentifera + Sclerolinum (= Monilifera) than to Frenulata. The intraepidermal nervous system with widely separated nerve cords, double brain commissures, double palp nerves and other traits found in Osedax can all be traced to represent ancestral states of Siboglinidae. A broader comparison of the nervous system and body regions across Osedax and other siboglinids allows for a reinterpretation of the anterior body region in the group.

An inordinate fondness for Osedax (Siboglinidae: Annelida): Fourteen new species of bone worms from California

“…Many Osedax species have palps that lack obvious pinnules. The dorsal placement of the oviduct reflects the reorientation of Osedax as reported in Huusgaard et al (2012) and Worsaae et al (2016).…”

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

“…In numerous annelids the neurite bundles of the VNC are located ventro-laterally in early developmental stages (and in several lineages of interstitial or meiofaunal annelids), but mid-ventrally in adults [21,68,[82][83][84]. Regardless of the annelid sister group a positional shift of the lateral neurite bundles towards the ventral midline has to be assumed to have evolved in the stem lineage of Annelida.…”

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.…”