Ecological genomics of an intertidal marine snail: Population structure and local adaptation to heat stress in Chlorostoma (formerly Tegula) funebralis

The intertidal marine snail Chlorostoma (formerly Tegula) funebralis has a wide geographic distribution, and across this range populations are exposed to large variations in temperature. Southern California (USA) populations generally occupy warmer climates and are presumably exposed to high air temperatures during low tides more often than northern California populations. C. funebralis' broad, thermally heterogeneous geographic range could promote local adaptation, or the fine-tuning of individuals to their local habitat via natural selection. However, this species also has pelagic larvae, and available genetic data have found no evidence for population structure, suggesting there may be extensive gene flow that could preclude local adaptation. Overall, the potential for adaptive differentiation in C. funebralis is unclear because the balance between selection for local adaptation and the rate of interpopulation gene flow is largely unknown. To address this issue phenotypic assays were used to identify initial evidence for local adaptation to heat stress in three northern and three southern California C. funebralis populations, and subsequently mRNA and DNA were sampled from these populations to examine transcriptome and genome -wide signatures of local adaptation. In the field, temperature data loggers were also deployed to explicitly quantify regional differences in thermal stress exposure among populations. The cumulative results of this work uncovered : (i) phenotypic evidence for local adaptation to heat stress between northern and southern California populations, with southern populations being more thermally tolerant than northern ones, (ii) region- specific transcriptomic responses to heat stress in northern and southern California, including unique gene expression strategies in southern populations that potentially confer higher thermal tolerance, (iii) differences in the frequency and magnitude of extreme thermal stress events in northern and southern California, and (iv) genomic evidence for ecological adaptation against a background of homogeneity in northern and southern California populations. Not only do these findings provide unique insights into region-specific responses of thermal stress response, but they also suggest that adaptation to local environmental differences can evolve despite a pelagic larval phase in C. funebralis. Accounting for intraspecific population variation in thermal tolerance may provide important insights for predicting how species distributions will respond to global warmin