Core Transcriptional Plasticity Pave the Way for Fish to Succeed in a High-CO₂ World

Ocean acidification (OA) can alter the physiological and behavioural traits of marine fishes, raising concerns about how wild species will adapt to rising pCO₂. Using natural volcanic CO₂ vents at White Island, New Zealand, as analogues for future OA conditions, we quantified behaviours in situ and sequenced the brain transcriptomes of four highly site-attached fish species from two vents and a nearby control site with ambient pCO₂, of which two species exhibit increased population densities at the vent. We found that two species showed changes in habitat preferences, and all four species with significant changes in gene expression related to circadian rhythm, visual perception, and energy metabolism at the vents. Strikingly, three differentially expressed genes, a heat shock protein (HS90A) and two immediate early genes (IEGs: JUN and FOS), were central regulators for transcriptional changes across all species at the vents. Within the circadian entrainment pathway, expression changes in opsins may act as a trigger, while core clock genes and IEGs function as downstream effectors, suggesting that elevated pCO₂ may reset the circadian clock in these fishes. Notably, the two species with increased populations at the vents exhibited distinct transcriptional responses in genes involved in calcium signalling, reproduction, intracellular pH regulation and energy metabolism. Together with convergent evolution in a calcium signalling gene and an HS90 facilitator, these molecular features may confer their reproduction advantages and ability to cope with elevated pCO₂. Our study provides novel insights into the molecular mechanisms underlying fish responses to OA and highlights key pathways that may support survival and ecological success under a naturally high-CO₂ world.