The contrasted evolutionary fates of deep-sea chemosynthetic mussels (Bivalvia, Bathymodiolinae)

International audienceBathymodiolinae are giant mussels that were discovered at hydrothermal vents and harboring chemosynthetic symbionts. Due to their close phylogenetic relationship with seep species and tiny mussels from organic substrates, it was hypothesized that they gradually evolved from shallow to deeper environments, and specialized in decaying organic remains, then in seeps, and finally colonized deep-sea vents. Here, we present a multigene phylogeny that reveals that most of the genera are polyphyletic and/or paraphyletic. The robustness of the phylogeny allows us to revise the genus-level classification. Organic remains are robustly supported as the ancestral habitat for Bathymodiolinae. However, rather than a single step toward colonization of vents and seeps, recurrent habitat shifts from organic substrates to vents and seeps occurred during evolution, and never the reverse. This new phylogenetic framework challenges the gradualist scenarios from shallow to deep. Mussels from organic remains tolerate a large range of ecological conditions and display a spectacular species diversity contrary to vent mussels, although such habitats are yet underexplored compared to vents and seeps. Overall, our data suggest that for deep-sea mussels, the high specialization to vent habitats provides ecological success in this harsh habitat but also brings the lineage to a kind of evolutionary dead end

A sad tale: has the small mussel Idas argenteus lost its symbionts?

Idas argenteus (Bivalvia: Mytilidae) belongs to a genus of mussels that are often associated with sunken wood and vertebrate bones in the deep sea. By contrast to other species currently included within the genus Idas and other related genera, such as Bathymodiolus, I. argenteus was documented to lack chemosynthetic symbionts bacterial symbionts in its gills. In the present study, new specimens are assigned to I. argenteus based on shell and soft parts analysis. Molecular data confirm the absence or low abundance of symbionts. Phylogeny based on five genes indicates that the symbiont-bearing I. washingtonius is the closest relative of I. argenteus. Symbiosis loss or extreme reduction is thus inferred to have occurred subsequent to the speciation event, 11–13 Mya. This is the first report of a loss of symbiosis within the clade of deep-sea chemosynthetic mussels

Integrative Biology of Idas iwaotakii (Habe, 1958), a 'Model Species' Associated with Sunken Organic Substrates

The giant bathymodioline mussels from vents have been studied as models to understand the adaptation of organisms to deep-sea chemosynthetic environments. These mussels are closely related to minute mussels associated to organic remains decaying on the deep-sea floor. Whereas biological data accumulate for the giant mussels, the small mussels remain poorly studied. Despite this lack of data for species living on organic remains it has been hypothesized that during evolution, contrary to their relatives from vents or seeps, they did not acquire highly specialized biological features. We aim at testing this hypothesis by providing new biological data for species associated with organic falls. Within Bathymodiolinae a close phylogenetic relationship was revealed between the Bathymodiolus sensu stricto lineage (i.e. "thermophilus'' lineage) which includes exclusively vent and seep species, and a diversified lineage of small mussels, attributed to the genus Idas, that includes mostly species from organic falls. We selected Idas iwaotakii (Habe, 1958) from this latter lineage to analyse population structure and to document biological features. Mitochondrial and nuclear markers reveal a north-south genetic structure at an oceanic scale in the Western Pacific but no structure was revealed at a regional scale or as correlated with the kind of substrate or depth. The morphology of larval shells suggests substantial dispersal abilities. Nutritional features were assessed by examining bacterial diversity coupled by a microscopic analysis of the digestive tract. Molecular data demonstrated the presence of sulphur-oxidizing bacteria resembling those identified in other Bathymodiolinae. In contrast with most Bathymodiolus s.s. species the digestive tract of I. iwaotakii is not reduced. Combining data from literature with the present data shows that most of the important biological features are shared between Bathymodiolus s.s. species and its sister-lineage. However Bathymodiolus s.s. species are ecologically more restricted and also display a lower species richness than Idas species

Scanning electron micrographs of the larval shell of a specimen of <i>Idas iwaotakii</i>.

<p>Pictures: (A) Dorsal view showing prodissoconch I (PI) and prodissoconch II (PII); the white arrow indicates the boundary between the dissoconch and prodissoconch, (B) Detail of PI; the grey arrow indicated of the boundary between PI and PII.</p

Exploration of the deep-sea fauna of Papua New Guinea

Little is known of New Guinea's deep benthic communities. In fall 2010, the Museum national d'Histoire naturelle, Institut de Recherche pour le Developpement, and University of Papua New Guinea spearheaded an international three-leg cruise, BioPapua, aimed at exploring the deep waters of eastern Papua New Guinea and its satellite islands. Special attention was given to faunal assemblages associated with sunken wood and decomposing vegetation as well as seamount summits and slopes. In this article, we review the information available on the deep ecosystems of Papua New Guinea and summarize preliminary results of the BioPapua cruise

Bayesian tree displaying bacterial symbionts based on the analysis of the 16S rRNA.

<p>Phylotypes associated with <i>I. iwaotakii</i> are shown in bold. Posterior probabilities (PP) and bootstrap values obtained from ML analysis are given above and below branches respectively. PP and bootstrap values lower than 0.90 and 50%, respectively, are not shown. The scale bar represents 0.5% estimated base substitution.</p

Gill filaments of <i>Idas iwaotakii</i>.

<p>(A) TEM view of gill filament of the lateral zone from a specimen of <i>I. iwaotakii</i> collected on wood off Vanuatu. Bacteria (black arrows) are located extracellularly in contact with microvilli. BL: blood lacuna; Lm: basal lamina. (B) Electron micrograph of the extracellular symbionts. Symbiotic bacteria possess a double membrane (white arrow) typical of Gram negative bacteria.</p