Origin, evolution, and adaptation of scaleworms from deep-sea chemosynthetic habitats

Scaleworms of the family Polynoidae (ca. 900 species worldwide) have colonized nearly all marine habitats, from the intertidal to the deep sea, from tropical to polar areas, and even chemosynthesis-based ecosystems. In this latter habitat, scaleworms represent nearly 10% of all invertebrate endemic species described so far, and in the world all areas harbor at least one species. These invertebrates are therefore very good candidates to study the colonization of the deep-sea, of chemosynthetic habitats, and the adaptations required to colonize these habitats. They also provide a speciose group that allows us to study the evolution of adaptations that were necessary to cope with the challenging conditions that are found at vents.
We produced a phylogeny of about 60 species, including seep, vent, and organic fall species, in addition to deep-sea and littoral species. Data show at least 5 events of colonization of the deep sea, among which two lineages lead to species collected at vents and seeps. In the general deep-sea, three lineages of Harmothoe or Harmothoe-like species are found, and these fall within a very diverse group that includes shallow-water species. The subfamily Iphioninae diverged into a chemosynthetic-specific lineage comprising sunken wood and vent species. Finally, most vent- and seep-endemic species form a monophyletic group that suggests a single colonization event for this diversified taxonomic group. Pairs of species from Juan de Fuca and the East Pacific Rise allowed us to calibrate the molecular clock and revealed that the original colonization event for vent- and seep-endemic monophyletic group occurred about 55 million years ago, following the last global deep-sea anoxic event. Interestingly, the original divergence of the chemosynthetic lineage of the Iphioninae and of the deep-sea Harmothoe-like also occurred at that time.
In this phylogenetic framework, we studied adaptations to low oxygen and high temperature. Adaptations to low oxygen can be studied at different organizational levels (from the morphology of the species to the molecular level). In particular, species with branchiae are only found in species from chemosynthetic habitats but not all species possess branchiae, and these features seem to have arisen twice. All the vent species (except for the Iphioninae) however possess hemoglobins in their coelomic species, suggesting that hemoglobin was already present in the common ancestor to all these species. When considering species from homologous microhabitats, branchiate species tend to have a lower hemoglobin concentration but all these hemoglobins have a high affinity for oxygen compared to non-vent species. We used a high-throughput transcriptome sequencing approach in 13 species from contrasted habitats to determine general trends in molecular adaptations and also used a targeted-gene approach in a larger number of species to improve the phylogenetic context and better understand the history of these adaptations. A targeted study of adaptation to temperature regimes was performed through the properties of the enzyme cytoplasmic malate dehydrogenase in response to temperature variations.

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Station Biologique de Roscoff - CNRS/UPMC
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Evolutionary history (fossil and molecular data)
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