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Abstract Adaptive evolution and phenotypic plasticity will fuel resilience in the geologically unprecedented warming and acidification of the earth’s oceans, however, we have much to learn about the interactions and costs of these mechanisms of resilience. Here, using 20 generations of experimental evolution followed by three generations of reciprocal transplants, we investigated the relationship between adaptation and plasticity in the marine copepod,Acartia tonsa, in future global change conditions (high temperature and high CO₂). We found parallel adaptation to global change conditions in genes related to stress response, gene expression regulation, actin regulation, developmental processes, and energy production. However, reciprocal transplantation showed that adaptation resulted in a loss of transcriptional plasticity, reduced fecundity, and reduced population growth when global change-adapted animals were returned to ambient conditions or reared in low food conditions. However, after three successive transplant generations, global change-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 that while plasticity facilitated initial survival in global change conditions, it eroded after 20 generations as populations adapted, limiting resilience to new stressors and previously benign environments. 

Abstract Colonization of new environments can lead to population bottlenecks and rapid phenotypic evolution that could be due to neutral and selective processes. Exotic populations of the bull‐headed dung beetle (Onthophagus taurus) have differentiated in opposite directions from native beetles in male horn‐to‐body size allometry and female fecundity. Here we test for genetic and transcriptional differences among two exotic and one nativeO. tauruspopulations after three generations in common garden conditions. We sequenced RNA from 24 individuals for each of the three populations including both sexes, and spanning four developmental stages for the two exotic, differentiated populations. Identifying 270,400 high‐quality single nucleotide polymorphisms, we revealed a strong signal of genetic differentiation between the three populations, and evidence of recent bottlenecks within and an excess of outlier loci between exotic populations. Differences in gene expression between populations were greatest in prepupae and early adult life stages, stages during which differences in male horn development and female fecundity manifest. Finally, genes differentially expressed between exotic populations also had greater genetic differentiation and performed functions related to chitin biosynthesis and nutrient sensing, possibly underlying allometry and fecundity trait divergences. Our results suggest that beyond bottlenecks, recent introductions have led to genetic and transcriptional differences in genes correlated with observed phenotypic differences.