The colonisation of hydrothermal vents by complex life: a natural experiment in macroevolution

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Our proposal unites a multidisciplinary team of researchers from mineralogy, palaeontology, deep-sea biology and genetics to provide an integrated picture of when and how some of the most remarkable environments on our planet were colonised by highly-specialised animals, and inform modern deep-sea conservation challenges.The discovery of hydrothermal vents in the deep sea during the late 1970s revolutionised our understanding of the limits of life on our planet. These explorations uncovered incredibly lush ecosystems supported by chemosynthesis, a carbon-fixation process previously deemed insignificant, and faunas with many novel adaptations to surviving in this dark habitat characterised by the ejection of extremely hot, toxic fluids from the seafloor. Despite their seemingly-hostile conditions, we now know that animals have thrived around vents for at least 440 million years, and that diverse taxonomic lineages have continually adapted to this environment over the course of Earth's history. Surprisingly, rather than functioning as evolutionary refuges in which ancient relict faunas have survived in isolation from large-scale environmental changes, evolution at vents appears to have occurred numerous times. This suggests that vents have an intriguing role as incubators of evolutionary novelty, their importance in evolution also highlighted by theories that life itself originated within this setting.Since their initial exploration, significant milestones have been achieved in surveying these ecosystems and in understanding the intimate interactions that modern vent faunas have with the microorganisms that support them. However, answers to fundamental questions of when animals first transitioned to occupy this environment, the processes driving the adaptation of new vent animals and the biological basis for vent colonisation are still lacking. A grasp of these principles is vitally important to understanding how animals adapt to unstable temperature regimes, and of how large-scale environmental changes affect the deep sea, the world's largest ecosystem. This is particularly pertinent today as the deep sea is increasingly affected by human activities, but how it responds to impacts such as climate change and mining operations is unknown.To gain vital evolutionary insights into the colonisation of hydrothermal vents, both in the modern ocean and throughout Earth history, we propose a comprehensive research programme guided by four hypotheses: H1) animals colonised hydrothermal vent environments soon after the Cambrian Explosion of life; H2) new vent habitat formation has repeatedly driven vent animal evolution over time; H3) ancient vent animals exhibited similar associations with microorganisms to modern vent animals to survive within harsh vent environments; and H4) adaptation to vent environmental regimes is evolutionarily rapid.We will assemble primary data for this project from field studies of key geological localities in Norway, Canada and Tasmania, which likely contain the oldest known bone-fide vent animals, and the southern Ural Mountains where a remarkable 100 million year fossil history of ancient vents is preserved. Together, these regions contain some of the best-preserved ancient hydrothermal vent deposits in the world. Collected fossil samples will be subjected to new detailed palaeontological investigations, and high resolution sulphur isotopic analyses. To investigate recent and ongoing adaptation at modern hydrothermal vents we will work on samples of traditional non-vent fauna that we can observe colonising new hydrothermal systems, using advanced DNA techniques.