Extreme Environmental Variability Induces Frontloading of Coral Biomineralisation Genes to Maintain Calcification Under <scp>pCO₂</scp> Variability

Corals residing in habitats that experience high-frequency seawater pCO₂ variability may possess an enhanced capacity to cope with ocean acidification, yet we lack a clear understanding of the molecular toolkit enabling acclimatisation to environmental extremes or how life-long exposure to pCO₂ variability influences biomineralisation. Here, we examined the gene expression responses and micro-skeletal characteristics of Pocillopora damicornis originating from the reef flat and reef slope of Heron Island, southern Great Barrier Reef. The reef flat and reef slope had similar mean seawater pCO₂, but the reef flat experienced twice the mean daily pCO₂ amplitude (range of 797 v. 399 μatm day^-1, respectively). A controlled mesocosm experiment was conducted over 8 weeks, exposing P. damicornis from the reef slope and reef flat to stable (218 ± 9) or variable (911 ± 31) diel pCO₂ fluctuations (μatm; mean ± SE). At the end of the exposure, P. damicornis originating from the reef flat demonstrated frontloading of 25% of the expressed genes regardless of treatment conditions, suggesting constitutive upregulation. This included higher expression of critical biomineralisation-related genes such as carbonic anhydrases, skeletal organic matrix proteins, and bicarbonate transporters. The observed frontloading corresponded with a 40% increase of the fastest deposited areas of the skeleton in reef flat corals grown under non-native, stable pCO₂ conditions compared to reef slope conspecifics, suggesting a compensatory response that stems from acclimatisation to environmental extremes and/or relief from stressful pCO₂ fluctuations. Under escalating ocean warming and acidification, corals acclimated to environmental variability warrant focused investigation and represent ideal candidates for active interventions to build reef resilience while societies adopt strict policies to limit climate change.