Cross-talk between tissues is critical for intergenerational acclimation to environmental change in Acanthochromis polyacanthus

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Organisms’ responses to environmental changes involve complex, coordinated responses of multiple tissues and potential parental influences. Here using a multi-tissue approach we determine how variation in parental behavioural tolerance and exposure to elevated CO2 influences the developmental and intergenerational molecular responses of their offspring in the coral reef fish Acanthochromis polyacanthus to future ocean acidification (OA) conditions. Gills and liver showed the highest transcriptional response to OA in juvenile fish regardless of parental OA conditioning, while the brain and liver showed the greatest intergenerational acclimation signals. Developmentally induced signals of OA, such as altered neural function in the brain, were restored to control levels after intergenerational exposure. Intergenerational CO2 exposure also enabled the offspring to adjust their metabolic processes, potentially allowing them to better meet the energetic demands of a high CO2 environment. Furthermore, offspring of OA-exposed parents differentially expressed a new complement of genes, which may facilitate intergenerational acclimatory responses. A genetic component of intergenerational plasticity also played a crucial role, with the parental behavioural phenotype largely determining the offspring’s transcriptional signals. Overall, our results reveal tissue-specific transcriptional changes underlying intergenerational plastic responses to elevated CO2 exposure, enhancing understanding of organismal acclimation to OA throughout the whole body.