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

Justine Thubaut,Corinne Cruaud,Sarah Samadi,Nicolas Puillandre,Baptiste Faure

doi:10.1002/ece3.749

Abstract

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.

Highlights

The exploration of the deep sea is relatively recent and many gaps remain in basic knowledge of marine biodiversity regarding taxonomy, geographic distribution, or ecology (Costello et al 2010)
Phylogenetic relationships among mytilids associated with deep-sea reducing habitats and genus-level classification
Including more taxa and more genes, we significantly improved the resolution of phylogenetic relationships among deep-sea mussels, both for many of the deeper nodes and for some of the internal nodes

Summary

Introduction

The exploration of the deep sea is relatively recent and many gaps remain in basic knowledge of marine biodiversity regarding taxonomy, geographic distribution, or ecology (Costello et al 2010). Marine biologists are focused on a few emblematic environments such as Antarctic biota or hydrothermal vents which are characterized by peculiar physical and chemical conditions that represent physiological challenges for organisms. The consequence of such knowledge gaps is that uncommon and spectacular phenotypic features or behaviors are interpreted, under the Panglossian paradigm (Gould and Lewontin 1979), as adaptations to these peculiar environmental conditions. To disentangle adaptive evolution from phylogenetic inertia the diversity of the related organisms should be covered taxonomically, geographically, and ecologically (Van Buskirk 2009). Because taxon sampling strongly affects the evolutionary inferences drawn from phylogenetic trees (Heath et al 2008), closely related taxa, from others habitats and/or other regions, should be included in the phylogenetic analyses

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