Adaptive radiation of chemosymbiotic deep-sea mussels

Abstract

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.

Adaptation to deep-sea chemosynthetic environments as revealed by mussel genomes

“…Using the lophotrochozoan tree as a reference, the time of divergence between B. platifrons and M. philippinarum was estimated to be around 110.4 million years ago (Ma), with a 95% confidence interval of 52.4-209.7 Ma (Fig. 2b), which is close to the upper age limit of deep-sea symbiotic mussels (102 Ma) previously estimated using five genes 14 . This result supports the hypothesis that the ancestors of modern deep-sea mussels might have experienced an extinction event during the global anoxia period that has been associated with the Palaeocene-Eocene thermal maximum at around 57 Ma 15 .…”

Did shifting seawater sulfate concentrations drive the evolution of deep-sea methane-seep ecosystems?

“…However, the only study on vent and seep clades to date that attempted to estimate the impact of extinction events on molecular diversification rates found little evidence for extinction at the PETM [23]. Furthermore, several apparently seep-restricted taxa, including the large abyssochrysoid Ascheria and Humptulipsia, survived both the end-Cretaceous mass extinction and the PETM [28,40,41], providing further evidence against a major role of extinction events in shaping the vent and seep fauna.…”

“…These range from external bacteria farming to highly integrated, intracellular symbioses, and the reduced chemicals for the symbionts are taken up from the water column, from the sediment, during continuous movements between oxic and anoxic environments, and bacterial growth can be supported by the active pumping of oxidized compounds into anoxic sediment, as in vestimentiferan tube worms [2]. We are only beginning to understand the origin, timing and triggers of these adaptations [23]. Shifting redox boundaries in the sediment through Earth's history, for example, in response to shifting sulfate concentrations, may well have played a significant role in this context.…”

Population structure and connectivity in Indo-Pacific deep-sea mussels of the Bathymodiolus septemdierum complex

“…1) and dominate both biomass and community dynamics (e.g., Sen et al 2014). More than 50 species (named and unnamed operational taxonomic units) are presently recognized (Lorion et al 2013), where species currently placed in the genus Bathymodiolus are the most diverse at hydrothermal vents.…”