Rapid evolution fuels transcriptional plasticity to ocean acidification

Abstract
Ocean acidification (OA) is postulated to affect the physiology, behavior, and life-history of marine species, but potential for acclimation or adaptation to elevated pCO2 in wild populations remains largely untested. We measured brain transcriptomes of six coral reef fish species at a natural volcanic CO2 seep and an adjacent control reef in Papua New Guinea. We show that elevated pCO2 induced common molecular responses related to circadian rhythm and immune system but different magnitudes of molecular response across the six species. Notably, elevated transcriptional plasticity was associated with core circadian genes affecting the regulation of intracellular pH and neural activity in Acanthochromis polyacanthus. Gene expression patterns were reversible in this species as evidenced upon reduction of CO2 following a natural storm-event. Compared with other species, Ac. polyacanthus has a more rapid evolutionary rate and more positively selected genes in key functions under the influence of elevated CO2, thus fueling increased transcriptional plasticity. Our study reveals the basis to variable gene expression changes across species, with some species possessing evolved molecular toolkits to cope with future OA.

Citation
Kang, J., Nagelkerken, I., Rummer, J. L., Rodolfo-Metalpa, R., Munday, P. L., Ravasi, T., & Schunter, C. (2022). Rapid evolution fuels transcriptional plasticity to ocean acidification. Global Change Biology. Portico. https://doi.org/10.1111/gcb.16119

Acknowledgements
King Abdullah University of Science and Technology, Grant/Award Number: OSR-2015-CRG4-2541; The Okinawa Institute of Science and Technology Graduate University; the French National Research Agency, Grant/Award Number: ANR15CE02-0006- 01 and ANR-17- ERC2- 0009; the University of Hong Kong start- up grant; the Australian Research Council (ARC) and ARC Centre of Excellence for Coral Reef Studies, Grant/Award Number: FT120100183 We are grateful to the local communities for access to their reef and to the National Research Institute and the Milne Bay Provincial Research Committee for approval to conduct research at this site. Thanks to Prof. Ralph Mana (School of Natural and Physical Sciences, University of Papua New Guinea) for his invaluable support to obtain PNG permits. We are grateful to the population of the Upa-Upasina Reef in Milne Bay Province, for allowing us to conduct the study on their reefs, and to the National Research Institute, the Milne Bay Provincial Research Committee, the New Ireland Provincial Administration, and the Conservation and Environment Protection Authority of Papua New Guinea for permits. We also thank the captain and crew of the MV Chertan for logistical support during the expedition. This study was supported by the Office of Competitive Research Funds OSR-2015-CRG4-2541 from the King Abdullah University of Science and Technology (T.R., P.L.M., C.S., J.L.R.), the University of Hong Kong start-up grant to C.S. (C.S., J.L.K.), the Australian Research Council (ARC) and ARC Centre of Excellence for Coral Reef Studies (P.L.M., J.L.R.), and The Okinawa Institute of Science and Technology Graduate University (T.R.). I.N. was supported by an ARC Future fellowship (grant no. FT120100183). R.R-M was supported by the French National Research Agency (ANR, project CARIOCA no. ANR15CE02-0006-01, and ANR-17-ERC2-0009). This project was completed under approval of the James Cook University animal ethics committee (A2534) and according to the University’s animal ethics guidelines. We thank the Molecular Ecology and Evolution lab at HKU for fruitful discussions and support.

Publisher
Wiley

Journal
Global Change Biology

DOI
10.1111/gcb.16119

Additional Links
https://onlinelibrary.wiley.com/doi/10.1111/gcb.16119

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