Genetic assimilation and accommodation shape adaptation to heat stress in a splash pool copepod

ABSTRACT Understanding how organisms respond to variable environments is becoming increasingly important in our rapidly changing world. Beyond genetic adaptation, plastic responses to the environment can alter phenotypes and fitness, ultimately driving evolution. However, the interaction between plasticity and adaptation during environmental change is complex and hard to measure in natural systems. Here, we used two populations of Tigriopus californicus copepods, a thermally tolerant southern population and a thermally sensitive northern population, to conduct a fully factorial split brood experiment where we exposed animals as larvae and adults to either a sublethal heat stress or control (no heat treatment) before measuring heat tolerance and gene expression patterns. We found that increased thermal tolerance across populations came at the expense of physiological plasticity and evolved through higher baseline expression of heat stress response genes across environmental contexts as well as increased gene expression plasticity in response to heat stress. In the thermally sensitive northern population, developmental exposure to heat stress led to higher adult tolerance and lower physiological plasticity underpinned by higher gene expression plasticity. Importantly, we found that the same set of genes were largely responsible for both the evolved higher tolerance in the southern population and the developmentally induced tolerance in the northern population suggesting that in this system, a shared molecular response contributes to acclimation and adaptation across both populations. These results link existing physiological plasticity with long-term evolutionary responses providing insight into how these populations will adapt and respond to future environmental change. SIGNIFICANCE Understanding plastic and evolutionary responses to dynamic environments is critical to anticipating species’ vulnerability to climate change. In this study, we compared gene expression and physiological responses to heat stress across two populations of a marine copepod that differ in thermal tolerance to investigate mechanisms of adaptation. We found evidence for plasticity-led evolution in this system, with the same set of genes contributing to long-term evolutionary changes across populations and to short-term physiological adjustments within populations. Our results suggest that populations with a reservoir of plasticity have a greater potential to evolve as the climate continues to warm, but that there may be a limit to this adaptive capacity.