Loss and recovery of transcriptional plasticity after long-term adaptation to global change conditions in a marine copepod

Adaptive evolution from standing genetic variation and physiological plasticity will fuel resilience in the geologically unprecedented warming and acidification of the earths oceans. For marine animals, however, we have much to learn about the mechanisms, interactions, and costs of adaptation. Here, using 20 generations of experimental evolution followed by three generations of reciprocal transplantation, we investigate the relationship between adaptation and plasticity in the marine copepod, Acartia tonsa, in future greenhouse conditions (high temperature, high CO2). We find highly parallel genetic adaptation to greenhouse conditions in genes related to stress response, gene expression regulation, actin regulation, developmental processes, and energy production. However, reciprocal transplantation showed that genetic adaptation resulted in a loss of transcriptional plasticity, reduced fecundity, and reduced population growth when greenhouse animals were returned to ambient conditions or reared in low food conditions, suggestive of genetic assimilation after 20 generations of adaptation. Despite the loss of plasticity at F21, after three successive transplant generations, greenhouse-adapted animals were able to match the ambient-adaptive transcriptional profile. Concurrent changes in allele frequencies and erosion of nucleotide diversity suggest that this recovery occurred via adaptation back to ancestral conditions. These results demonstrate the power of experimental evolution from natural populations to reveal the mechanisms, timescales of responses, consequences, and reversibility of complex, physiological adaptation. While plasticity facilitated initial survival in global change conditions, it eroded after 20 generations as populations genetically adapted, limiting resilience to new stressors and previously benign environments.