Timing specific parental effects of ocean warming in a coral reef fish

Population and species persistence in a rapidly warming world will be determined by an organisms’ ability to acclimate to warmer conditions, especially across generations. There is potential for transgenerational acclimation, but the importance of ontogenetic timing in the transmission of environmentally induced parental effects remains mostly unknown. We aimed to disentangle the contributions of two critical ontogenetic stages (juvenile development and adult reproduction) to transgenerational plasticity, by exposing the coral reef fish Acanthochromis polyacanthus to simulated ocean warming with natural diel thermal fluctuations across two generations. By using hepatic transcriptomics, we discovered that the developmental environment of the offspring themselves had little effect on their acclimation potential at 2.5 months of life. Instead, the developmental experience of parents increased regulatory RNA production and protein synthesis, which could improve the offspring’s response to warming. Conversely, reproduction in warmer water elicited stress response mechanisms, with suppression of translation and mitochondrial respiration. Mismatches between temperatures in the parental ontogenetic thermal experience deeply affected offspring gene expression profiles, and detrimental effects were also evident when warming occurred both during parents’ development and reproduction. This study reveals that the previous generation’s developmental temperature contributes substantially to thermal acclimation potential during early life, however prolonged heat stress will likely have adverse effects on the species’ persistence.