The Contrasted Evolutionary Fates of Deepsea
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The contrasted evolutionary fates of deep-sea chemosynthetic mussels (Bivalvia, Bathymodiolinae)a Justine Thubaut1, Nicolas Puillandre1, Baptiste Faure2,3, Corinne Cruaud4 & Sarah Samadi1 1Departement Systematique et Evolution, Museum National d’Histoire Naturelle, Unite Mixte de Recherche 7138 (UPMC-IRD-MNHN-CNRS), “Systematique Adaptation et Evolution”, 75005 Paris, France 2Station Biologique de Roscoff, Unite Mixte de Recherche 7127, Centre National de la Recherche Scientifique, Universite Pierre et Marie Curie, 29680 Roscoff, France 3Biotope, Service Recherche et Developpement, BP58 34140 Meze, France 4Genoscope, CP 5706, 91057 Evry, France Keywords Abstract Bathymodiolinae, chemosynthetic ecosystem, deep-sea, evolution. Bathymodiolinae are giant mussels that were discovered at hydrothermal vents and harboring chemosynthetic symbionts. Due to their close phylogenetic rela- Correspondence tionship with seep species and tiny mussels from organic substrates, it was Departement Systematique et Evolution, hypothesized that they gradually evolved from shallow to deeper environments, Museum National d’Histoire Naturelle, Unite Mixte de Recherche 7138 (UPMC-IRD-MNHN- and specialized in decaying organic remains, then in seeps, and finally colonized CNRS), “Systematique, Adaptation et deep-sea vents. Here, we present a multigene phylogeny that reveals that most Evolution,” 75005 Paris, France. of the genera are polyphyletic and/or paraphyletic. The robustness of the Tel: +33 (0)1 40 79 37 43; Fax: +33 (0)1 40 phylogeny allows us to revise the genus-level classification. Organic remains are 79 38 44; E-mail: [email protected] robustly supported as the ancestral habitat for Bathymodiolinae. However, Funding Information rather than a single step toward colonization of vents and seeps, recurrent habi- This study was supported by a grant of the tat shifts from organic substrates to vents and seeps occurred during evolution, Fondation pour la Recherche sur la and never the reverse. This new phylogenetic framework challenges the gradual- Biodiversite (FRB AAP-IN-2009-009), the ist scenarios “from shallow to deep.” Mussels from organic remains tolerate a “Consortium National de Recherche en large range of ecological conditions and display a spectacular species diversity Genomique”, and the “Service de contrary to vent mussels, although such habitats are yet underexplored com- Systematique Moleculaire” of the Museum National d’Histoire Naturelle (CNRS UMS pared to vents and seeps. Overall, our data suggest that for deep-sea mussels, 2700), part of the agreement n°2005/67 the high specialization to vent habitats provides ecological success in this harsh between the Genoscope and the Museum habitat but also brings the lineage to a kind of evolutionary dead end. National d’Histoire Naturelle on the project “Macrophylogeny of life” directed by Guillaume Lecointre and by the network “Bibliotheque du Vivant” funded by the CNRS, the Museum National d’Histoire Naturelle, the INRA and the CEA (Genoscope).” This work is part of the projects @ SPEED-ID “Accurate SPEciEs Delimitation and IDentification of eukaryotic biodiversity using DNA markers” proposed by F-BoL, the French Barcode of life initiative. Received: 3 April 2013; Revised: 22 July 2013; Accepted: 24 July 2013 Ecology and Evolution 2013; 3(14): 4748– 4766 doi: 10.1002/ece3.749 aAll the new sequences are submitted to GenBank, and the accession numbers should arrive shortly. 4748 ª 2013 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. J. Thubaut et al. Evolutionary History of Deep-Sea Mussels Introduction gradual evolution toward specialization from shallow water environments to cold seeps and finally to deep-sea The exploration of the deep sea is relatively recent and many vents. Then, the evolutionary scenario was refined (Distel gaps remain in basic knowledge of marine biodiversity et al. 2000), based on a molecular phylogenetic analysis regarding taxonomy, geographic distribution, or ecology that included some small mussels sampled on organic (Costello et al. 2010). Moreover, marine biologists are remains, sunken at the deep-sea floor. This new scenario focused on a few emblematic environments such as Antarctic introduced a “wooden step” that predates the colonization biota or hydrothermal vents which are characterized by pecu- of deep-sea seeps and vents. Recently, several studies liar physical and chemical conditions that represent physio- (Duperron et al. 2009) revealed the presence of sulfide- logical challenges for organisms. The consequence of such oxidizing bacteria in the gills of all examined deep-sea knowledgegapsisthatuncommonandspectacular mussels sampled on organic remains. Several phylogenetic phenotypic features or behaviors are easily interpreted, under studies also confirmed that the evolutionary history of the Panglossian paradigm (Gould and Lewontin 1979), as vent and seep mussels is tightly tied to that of the small adaptations to these peculiar environmental conditions. For mussels sampled on organic falls of the deep sea and that example, it was speculated that the gigantism of pycnogonids the small mussels associated with organic falls should be from Antarctica is adaptive and stems from high polar oxygen included within Bathymodiolinae (Samadi et al. 2007; Lo- availability coupled with low metabolic rates (Chapelle and rion et al. 2009, 2010). These results, although still preli- Peck 1999), but physiological studies have not confirmed minary, suggest a more complex evolutionary history than this hypothesis (Woods et al. 2009), which remains contro- gradual evolution (i.e., from shallow to deep or from stan- versial (Klok 2009). An alternative explanation might be dard oceanic conditions to “extreme” physical and chemi- that it results from phylogenetic contingency rather than cal conditions). However, many studies (Jones et al. 2006; from adaptive processes. However, to disentangle adaptive Kyuno et al. 2009; Fujiwara et al. 2010; Miyazaki et al. evolution from phylogenetic inertia the diversity of the 2010) still suggest that gradual evolutionary scenarios in related organisms should be covered taxonomically, geo- which, for example, the presence of intracellular chemo- graphically, and ecologically (Van Buskirk 2009). For synthetic bacteria is interpreted as a “final step” toward example, when sampling is biased toward a given habitat, the adaptation to extreme environments (c.f. Miyazaki characters shared by the taxa from this habitat may be mis- et al. 2010). takenly interpreted as an adaptation to it. Thus, because Presently, most of the studies on Bathymodiolinae, taxon sampling strongly affects the evolutionary inferences focusing either on biology, physiology, or behavior, offer drawn from phylogenetic trees (Heath et al. 2008), closely adaptive interpretations of biological features that do not related taxa, from others habitats and/or other regions, take the most recent phylogenetic results into account should be included in the phylogenetic analyses. (Dixon et al. 2004; Hardivillier et al. 2004; Pruski and We here focus on the Bathymodiolinae mussels, often Dixon 2007; Serafim et al. 2008; Mestre et al. 2009; Betten- considered as model organisms in the study of adaptation court et al. 2010). For example, to unravel genes specifically to extreme marine environments (Kadar et al. 2005; Kadar involved in hydrostatic pressure and chemosynthetic envi- and Powell 2006; Lallier 2006). Bathymodiolinae were first ronmental adaptations, Bettencourt et al. (2010) compared described from deep-sea hydrothermal vents that, con- the transcriptome profiles of Bathymodiolus azoricus and trasting with the more generally oligotrophic deep-sea Mytilus galloprovincialis. The underlying assumption justi- habitats, are characterized by extreme physicochemical fying the adaptive inferences is that these two species are conditions associated with an abundant and unique fauna. “closely related Mytilid family members living in very dis- Soon after the discovery of this environment, the impres- tinct marine habitat.” However, a recent study (Lorion sive productivity was explained by the chemosynthetic et al. 2010) confirmed that many biological features – such process that sustains primary production in absence of as the presence of chemosynthetic bacteria – are shared by light both through free-living bacteria, grazed by animals, more closely related mussels that do not inhabit the harsh and through bacteria living in symbiosis with metazoans vent habitat. Thus, adaptive inferences must be based on (Jannasch 1985). Consequently, among the biological fea- comparative approaches with these closest relatives rather tures of Bathymodiolus (the first genus described in the than with the poorly related shallow water Mytilus species. Bathymodiolinae to which are attributed most of the giant The main goal of this study was thus to clarify the phylo- mussels sampled at hydrothermal vents), the symbiosis genetic relationships among the Bathymodiolinae sensus with chemosynthetic bacteria is often considered as the lato (i.e., including both Bathymodiolinae sensus stricto and key adaptation that explains the ecological success of these the small mussels from organic falls included in the same mussels in these harsh habitats. This success was first monophyletic clade) from deep-sea