Complementary genetic and epigenetic changes facilitate rapid adaptation to multiple global change stressors

Abstract To persist in the geologically unprecedented rates of global change, populations can adapt or acclimate. However, how these mechanisms of resilience interact, particularly the role of epigenetic variation in long-term adaptation, is unknown. To address this gap, we experimentally evolved the foundational marine copepod Acartia tonsa for 25 generations under ocean acidification, warming, their combination, and control conditions then measured epigenomic, genomic, and transcriptomic responses. We observed clear and consistent epigenomic and genomic divergence between treatments, with epigenomic divergence concentrated in genes related to stress response and the regulation of transposable elements. However, epigenetic and genetic changes occurred in different regions of the genome such that regions with significant methylation divergence had 2-2.5 fold lower F ST than regions without methylation divergence. This negative relationship between epigenetic and genetic divergence could be driven by local inhibition of one another or distinct functional targets of selection. In contrast, epigenetic divergence was positively linked to gene expression divergence, indicating that epigenetic changes may facilitate phenotypic change. Taken together, these results suggest that unique, complementary genetic and epigenetic mechanisms promote resilience to global change. Significance Statement Organisms must adapt or acclimate to survive global change, but how these processes interact and the role of epigenetic variation is unknown. To address these gaps, we experimentally evolved the marine copepod Acartia tonsa for 25 generations in global change conditions and measured their genomic, epigenomic, and gene expression responses. We found that both genetic and epigenetic changes contributed to resilience and were inversely related, acting in different regions of the genome. Epigenetic changes were functionally linked to the regulation of stress and transposable elements and correlated with shifts in gene expression. Therefore, the resilience of populations to ongoing global change is driven by the complementary contribution of both genetic and epigenetic mechanisms.