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      Description and morphology of the “Juan de Fuca vent mussel”, Benthomodiolus erebus sp. n. (Bivalvia, Mytilidae, Bathymodiolinae): “Phylogenetically basal but morphologically advanced”

      Zoosystematics and Evolution

      Pensoft Publishers

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          Abstract

          The Juan de Fuca vent mussel first found in 1990 is formally described as Benthomodiolus erebus sp. n. Comparisons are made with the three other species previously assigned to Benthomodiolus namely B. lignocola, B. geikotsucola and B. abyssicola. The anatomies of all four species are examined and are shown to share the arrangement of pedal and byssus musculature, having largely un-fused mantle margins and a hind gut with a very short loop. The ctenidia were examined using both light and scanning electron microscopy. B. erebus and B. geikotsucola were found to have lamellar filaments with extensive abfrontal expansion and fusion of the ascending and descending arms. In this there is similarity with Bathymodiolus. B. lignocola and B. abyssicola were found to have linear filaments with narrow abfrontal surfaces with little fusion. All four species were shown to have the abfrontal surfaces covered by polygonal cushions of microvilli although these were much less apparent in B. lignocola and B. abyssicola. Although Benthomodiolus was shown by a number of previous studies, using molecular data alone, to be phylogenetically basal to all other Bathymodiolinae the anatomy is highly adapted for chemosymbiosis. Species of Benthomodiolus are found on wood-falls, whale-falls and vent sites and thus mirror the habits of the Bathymodiolus/Idas clade.

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          Adaptive radiation of chemosymbiotic deep-sea mussels

          Adaptive radiations present fascinating opportunities for studying the evolutionary process. Most cases come from isolated lakes or islands, where unoccupied ecological space is filled through novel adaptations. Here, we describe an unusual example of an adaptive radiation: symbiotic mussels that colonized island-like chemosynthetic environments such as hydrothermal vents, cold seeps and sunken organic substrates on the vast deep-sea floor. Our time-calibrated molecular phylogeny suggests that the group originated and acquired sulfur-oxidizing symbionts in the Late Cretaceous, possibly while inhabiting organic substrates and long before its major radiation in the Middle Eocene to Early Oligocene. The first appearance of intracellular and methanotrophic symbionts was detected only after this major radiation. Thus, contrary to expectations, the major radiation may have not been triggered by the evolution of novel types of symbioses. We hypothesize that environmental factors, such as increased habitat availability and/or increased dispersal capabilities, sparked the radiation. Intracellular and methanotrophic symbionts were acquired in several independent lineages and marked the onset of a second wave of diversification at vents and seeps. Changes in habitat type resulted in adaptive trends in shell lengths (related to the availability of space and energy, and physiological trade-offs) and in the successive colonization of greater water depths.
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            The contrasted evolutionary fates of deep-sea chemosynthetic mussels (Bivalvia, Bathymodiolinae)a

            Bathymodiolinae 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.
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              Hydrothermal vents in turbidite sediments on a Northeast Pacific spreading centre: organisms and substratum at an ocean drilling site

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                Author and article information

                Journal
                Zoosystematics and Evolution
                ZSE
                Pensoft Publishers
                1860-0743
                1435-1935
                August 11 2015
                August 11 2015
                : 91
                : 2
                : 151-165
                Article
                10.3897/zse.91.5417
                © 2015
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