MicroRNA-mediated transgenerational plasticity reveals pathways for ocean warming resilience

With anthropogenic climate change driving unprecedented ocean warming and posing a major threat to marine organisms, phenotypic plasticity mediated by epigenetic mechanisms may enable acclimation and persistence across generations. MicroRNAs (miRNAs) are epigenetic regulators that have long been associated with maladaptive stress responses across generations, yet their role in facilitating transgenerational acclimation remains unexplored. To examine miRNAs’ role in transgenerational thermal plasticity, we conducted a fully factorial split-clutch design experiment in the coral reef fish Acanthochromis polyacanthus. Parents and offspring were exposed throughout development to control (+0°C) or elevated (+1.5°C) temperatures, and offspring hepatic miRNA and mRNA were profiled. We identified 678 miRNAs in A. polyacanthus , including 226 conserved and 452 novel sequences. Direct (developmental) and parental (transgenerational) warming caused similar numbers of miRNAs to alter expression, while mRNA expression was more strongly influenced by parental effects. The two parents had distinct effects on offspring miRNA-mRNA networks, with paternal warming mainly altering offspring metabolism and stress responses, while maternal exposure predominantly influencing immunity and tissue organization. Overall, mismatched parental temperatures created trade-offs in offspring, whereas congruent (biparental) warming led to a unique, non-additive, response with fewer miRNA changes and lack of stress pathway activation. Our findings reveal that miRNAs mediate both developmental and transgenerational plasticity, highlighting the capacity of transgenerational effects to influence climate resilience, while also emphasizing the necessity of accounting for both maternal and paternal contributions when predicting species’ adaptability to ocean warming.