Bone-Eating Worms Spread: Insights into Shallow-Water Osedax (Annelida, Siboglinidae) from Antarctic, Subantarctic, and Mediterranean Waters

Abstract

Osedax, commonly known as bone-eating worms, are unusual marine annelids belonging to Siboglinidae and represent a remarkable example of evolutionary adaptation to a specialized habitat, namely sunken vertebrate bones. Usually, females of these animals live anchored inside bone owing to a ramified root system from an ovisac, and obtain nutrition via symbiosis with Oceanospirillales gamma-proteobacteria. Since their discovery, 26 Osedax operational taxonomic units (OTUs) have been reported from a wide bathymetric range in the Pacific, the North Atlantic, and the Southern Ocean. Using experimentally deployed and naturally occurring bones we report here the presence of Osedax deceptionensis at very shallow-waters in Deception Island (type locality; Antarctica) and at moderate depths near South Georgia Island (Subantarctic). We present molecular evidence in a new phylogenetic analysis based on five concatenated genes (28S rDNA, Histone H3, 18S rDNA, 16S rDNA, and cytochrome c oxidase I–COI–), using Maximum Likelihood and Bayesian inference, supporting the placement of O. deceptionensis as a separate lineage (Clade VI) although its position still remains uncertain. This phylogenetic analysis includes a new unnamed species (O. ‘mediterranea’) recently discovered in the shallow-water Mediterranean Sea belonging to Osedax Clade I. A timeframe of the diversification of Osedax inferred using a Bayesian framework further suggests that Osedax diverged from other siboglinids during the Middle Cretaceous (ca. 108 Ma) and also indicates that the most recent common ancestor of Osedax extant lineages dates to the Late Cretaceous (ca. 74.8 Ma) concomitantly with large marine reptiles and teleost fishes. We also provide a phylogenetic framework that assigns newly-sequenced Osedax endosymbionts of O. deceptionensis and O. ‘mediterranea’ to ribospecies Rs1. Molecular analysis for O. deceptionensis also includes a COI-based haplotype network indicating that individuals from Deception Island and the South Georgia Island (ca. 1,600 km apart) are clearly the same species, confirming the well-developed dispersal capabilities reported in other congeneric taxa. In addition, we include a complete description of living features and morphological characters (including scanning and transmission electron microscopy) of O. deceptionensis, a species originally described from a single mature female, and compare it to information available for other congeneric OTUs.

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

“…1) and these did not differ fundamentally from the results reported by Taboada et al (2015), despite the exclusion of divergent outgroup sequences. The major clades within Osedax (as indicated in Figure 1) followed those delineated in previous studies Taboada et al 2015;Vrijenhoek et al 2009).…”

“…1) and these did not differ fundamentally from the results reported by Taboada et al (2015), despite the exclusion of divergent outgroup sequences. The major clades within Osedax (as indicated in Figure 1) followed those delineated in previous studies Taboada et al 2015;Vrijenhoek et al 2009). The new results showed that the western Atlantic species, Osedax '1335_61_2' (Sumida et al 2016), belongs in clade IV and it constituted a well-supported sister-group to Osedax frankpressi from California (Fig.…”

“…As with Taboada et al (2015), there was poor support for several nodes, the most notable being the grouping of clades I and II, as well as placing clades I, II and VI together (Fig. 1).…”

A new member of the genus Antarctonemertes (Hoplonemertea, Nemertea) from Antarctic waters

“…Whether this lack of variability in the haplotypes found in several years is a typical pattern for these species across their range or it is related to the characteristics of Deception Island (a natural harbour with a relatively low connection to the open sea; Lenn et al 2003), remains unclear. Interestingly, a previous study on the siboglinid annelid Osedax deceptionensis Taboada et al, 2013 at Deception Island found that the haplotype of a single specimen collected in 2010 did not match any of the 11 haplotypes (out of 18 individuals) reported in the same location two years later (Taboada et al 2015). However, O. deceptionensis has a lecithotrophic larval stage that confers this species remarkable dispersal abilities as opposed to Antarctonemertes species (Taboada et al 2015).…”

“…Interestingly, a previous study on the siboglinid annelid Osedax deceptionensis Taboada et al, 2013 at Deception Island found that the haplotype of a single specimen collected in 2010 did not match any of the 11 haplotypes (out of 18 individuals) reported in the same location two years later (Taboada et al 2015). However, O. deceptionensis has a lecithotrophic larval stage that confers this species remarkable dispersal abilities as opposed to Antarctonemertes species (Taboada et al 2015).…”