Rapid evolution fuels transcriptional plasticity to ocean acidification

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.