Abstract
BackgroundExtreme environments prompt the evolution of characteristic adaptations. Yet questions remain about whether radiations in extreme environments originate from a single lineage that masters a key adaptive pathway, or if the same features can arise in parallel through convergence. Species endemic to deep-sea hydrothermal vents must accommodate high temperature and low pH. The most successful vent species share a constrained pathway to successful energy exploitation: hosting symbionts. The vent-endemic gastropod genus Gigantopelta, from the Southern and Indian Oceans, shares unusual features with a co-occurring peltospirid, the ‘scaly-foot gastropod’ Chrysomallon squamiferum. Both are unusually large for the clade and share other adaptive features such as a prominent enlarged trophosome-like oesophageal gland, not found in any other vent molluscs.ResultsTransmission electron microscopy confirmed endosymbiont bacteria in the oesophageal gland of Gigantopelta, as also seen in Chrysomallon. They are the only known members of their phylum in vent ecosystems hosting internal endosymbionts; other vent molluscs host endosymbionts in or on their gills, or in the mantle cavity. A five-gene phylogenetic reconstruction demonstrated that Gigantopelta and Chrysomallon are not phylogenetically sister-taxa, despite their superficial similarity. Both genera have specialist adaptations to accommodate internalised endosymbionts, but with anatomical differences that indicate separate evolutionary origins. Hosting endosymbionts in an internal organ within the host means that all resources required by the bacteria must be supplied by the animal, rather than directly by the vent fluid. Unlike Chrysomallon, which has an enlarged oesophageal gland throughout post-settlement life, the oesophageal gland in Gigantopelta is proportionally much smaller in juveniles and the animals likely undergo a trophic shift during ontogeny. The circulatory system is hypertrophied in both but the overall size is smaller in Gigantopelta. In contrast with Chrysomallon, Gigantopelta possesses true ganglia and is gonochoristic.ConclusionsKey anatomical differences between Gigantopelta and Chrysomallon demonstrate these two genera acquired a similar way of life through independent and convergent adaptive pathways. What appear to be the holobiont’s adaptations to an extreme environment, are driven by optimising bacteria’s access to vent nutrients. By comparing Gigantopelta and Chrysomallon, we show that metazoans are capable of rapidly and repeatedly evolving equivalent anatomical adaptations and close-knit relationships with chemoautotrophic bacteria, achieving the same end-product through parallel evolutionary trajectories.
Highlights
Extreme environments prompt the evolution of characteristic adaptations
Our analysis clearly demonstrated that this suite of adaptations to a vent ecosystem has been convergently acquired in the two genera (Fig. 1)
We confirmed that the oesophageal gland in Gigantopelta chessoia does house endosymbiotic bacteria (Fig. 2), but comparative anatomy (Fig. 3) revealed substantial differences that belie the potential homology of these adaptive features
Summary
Extreme environments prompt the evolution of characteristic adaptations. Yet questions remain about whether radiations in extreme environments originate from a single lineage that masters a key adaptive pathway, or if the same features can arise in parallel through convergence. Animals inhabiting deepsea hydrothermal vents face high pressure, strong gradients of pH and temperature, hydrogen sulfide, methane, and heavy metals [1, 2] The foundation of these ecosystems is microbial chemosynthesis [3] and many endemic vent metazoans host symbiotic bacteria either on the body surface as epibonts (e.g., crustaceans Shinkaia, Rimicaris), or within their tissues as endosymbionts (e.g., siboglinid tubeworms Riftia, and molluscs Calyptogena, Bathymodiolus) [4]. Chemosynthesis generates energy through the oxidation of sulfide and methane, the key oxidant being oxygen in the surrounding water [5] These animals usually present conspicuous physiological and anatomical adaptations to serve the endosymbiont; for example siboglinid tubeworms have a specialised organ, the trophosome, to house their sulfur-oxidising bacteria and have haemoglobin that binds both oxygen and sulfur to supply the bacteria with its two key resources [6]. Hosting symbiotic bacteria is the unifying feature of vent-endemic primary consumers, and appears to be the singular constrained evolutionary pathway to successful exploitation of the energy from vents
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