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

BACKGROUND: Bone-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. RESULTS: The 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. CONCLUSIONS: Osedax 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

The neuroanatomy of the siboglinid Riftia pachyptila highlights sedentarian annelid nervous system evolution.

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

Distribution of Gutless Siboglinid Worms (Annelida, Siboglinidae) in Russian Arctic Seas in Relation to Gas Potential

In the Russian Arctic seas and adjacent areas of the Arctic basin, 120 sites of siboglinid records are currently known. Individuals belonging to 15 species have been collected. The largest number (49.2%) of records were made in the Barents Sea, followed by the Laptev Sea (37.5%) and the Arctic basin (10 records; 8.3%). No siboglinids have been reported from the Chukchi Sea. The largest number of species has been identified in both the Laptev Sea and Arctic basin (seven species each). Seventy-eight percent of the records were discovered at water depths down to 400 m. Many of the siboglinid records in the Arctic seas of Russia are associated with areas of high hydrocarbon concentrations. In the Barents Sea, Nereilinum murmanicum has been collected near the largest gas fields. The records of Oligobrachia haakonmosbiensis, N. murmanicum, Siboglinum ekmani, Siboglinum hyperboreum, Siboglinum norvegicum, as well as two undetermined species of siboglinids are associated with the marginal areas of bottom gas hydrates where methane emissions can occur. The Arctic seas of Russia feature vast areas of permafrost rocks containing gas hydrates flooded by the sea. Under the influence of river runoff, gas hydrates dissociate, and methane emissions occur. Crispabrachia yenisey and Galathealinum karaense were found in the Yenisei estuary, and O. haakonmosbiensis was found in the Lena estuary

Distribution of Gutless Siboglinid Worms (Annelida, Siboglinidae) in Russian Arctic Seas in Relation to Gas Potential

In the Russian Arctic seas and adjacent areas of the Arctic basin, 120 sites of siboglinid records are currently known. Individuals belonging to 15 species have been collected. The largest number (49.2%) of records were made in the Barents Sea, followed by the Laptev Sea (37.5%) and the Arctic basin (10 records; 8.3%). No siboglinids have been reported from the Chukchi Sea. The largest number of species has been identified in both the Laptev Sea and Arctic basin (seven species each). Seventy-eight percent of the records were discovered at water depths down to 400 m. Many of the siboglinid records in the Arctic seas of Russia are associated with areas of high hydrocarbon concentrations. In the Barents Sea, Nereilinum murmanicum has been collected near the largest gas fields. The records of Oligobrachia haakonmosbiensis, N. murmanicum, Siboglinum ekmani, Siboglinum hyperboreum, Siboglinum norvegicum, as well as two undetermined species of siboglinids are associated with the marginal areas of bottom gas hydrates where methane emissions can occur. The Arctic seas of Russia feature vast areas of permafrost rocks containing gas hydrates flooded by the sea. Under the influence of river runoff, gas hydrates dissociate, and methane emissions occur. Crispabrachia yenisey and Galathealinum karaense were found in the Yenisei estuary, and O. haakonmosbiensis was found in the Lena estuary

A tale of two tubeworms: taxonomy of vestimentiferans (Annelida: Siboglinidae) from the Mid-Cayman Spreading Centre

The vestimentiferan tubeworm genera Lamellibrachia and Escarpia inhabit deep-sea chemosynthesis-based ecosystems, such as seeps, hydrothermal vents and organic falls, and have wide distributions across the Pacific, Atlantic and Indian Oceans. In 2010–2012 during initial explorations of hydrothermal vents of the Mid-Cayman Spreading Centre (MCSC), both genera were found to co-occur at the Von Damm Vent Field (VDVF), a site characterised by diffuse flow, therefore resembling a ‘hydrothermal seep’. Here, we erect two new vestimentiferan tubeworm species from the VDVF, Lamellibrachia judigobini sp. nov. and Escarpia tritentaculata sp. nov. Lamellibrachia judigobini sp. nov. differs genetically and morphologically from other Lamellibrachia species, and has a range that extends across the Gulf of Mexico, MCSC, off Trinidad and Tobago, and Barbados, and also across both vents and seeps and 964–3304-m water depth. Escarpia tritentaculata sp. nov. is distinguished from other Escarpia species primarily based on morphology and is known only from vents of the MCSC at 2300-m depth. This study highlights the incredible habitat flexibility of a single Lamellibrachia species and the genus Escarpia, and historic biogeographic connections to the eastern Pacific for L. judigobini sp. nov. and the eastern Atlantic for E. tritentaculata sp. nov