Invasive species with native ranges spanning strong environmental gradients that establish in new habitats are particularly well-suited for examining the roles of selection and population history in rapid environmental adaptation, providing insight into potential evolutionary responses to climate change. The Atlantic oyster drill (Urosalpinx cinerea) is a marine snail with a native range spanning the strongest marine thermal gradient in the world that has established invasive populations on the U.S. Pacific coast. Here, we leverage this system using genome-wide SNPs and environmental data to examine invasion history and identify genotype-environment associations indicative of local adaptation across its native range, and then assess evidence for predicted allelic frequency shifts signaling rapid adaptation in invasive populations. We demonstrate strong genetic structuring among native regions aligned with life history expectations and identify southern New England as the source of invasive populations. We also identify putatively thermally adaptive loci across the native range, for which two invasive populations show significant divergence from source populations. However, we find no evidence of directional shifts in allele frequencies as would be predicted by environmental selection, suggesting that divergence is likely due to genetic drift rather than rapid adaptation. Alternatively, the success of new populations in environments differing from their origin may be due to relaxed selection pressures associated with more benign conditions, and/or standing capacity for phenotypic plasticity. This demonstrates the utility of invasive species for understanding evolutionary responses to changing environments, and the importance of considering population history and environmental selection pressures when evaluating adaptative capacity.

Adaptive phenotypes are shaped by a combination of genetic and environmental forces, and while the literature is rich with studies focusing on either genetics or environment contributions, those that consider both are rare. Here we utilize the cichlid oral jaw apparatus to fill this knowledge-gap. First, we employed RNA-seq in bony and ligamentous tissues important for jaw opening to identify differentially expressed genes between species and across foraging environments. Our foraging treatments were designed to force animals to employ either suction or biting/scraping, which broadly mimic pelagic or benthic modes of feeding. We found a large number of differentially expressed genes between species, and while we identified relatively few differences between environments, species differences were far more pronounced when reared in the pelagic versus benthic environment. Further, these data carried the signature of genetic assimilation, and implicated cell cycle regulation in shaping the jaw across species and environments. Next, we repeated the foraging experiment and performed ATAC-seq procedures on nuclei harvested from the same tissues. Cross-referencing results from both analyses revealed subsets of genes that were both differentially expressed and differentially accessible in either the pelagic (n=15) or the benthic environment (n=11), as well as loci where differences were robust to foraging environment (n=13). All in all, these data provide novel insights into the epigenetic, genetic, and cellular bases of species- and environment-specific bone shapes, as well as the evolution of phenotypic plasticity in this iconic model system.