Global climate change is threatening aquatic organisms with rapid changes in habitat salinity and temperature. In response to such changing conditions, adaptation could rescue populations from extinction. Gene flow is a key factor that could either promote or hinder local adaptation, with either beneficial or maladapted alleles immigrating from elsewhere. This interplay between local adaptation and gene flow has not been fully explored in passive dispersers, such as plankton. Thus, we investigated patterns of gene flow and genomic signatures of local adaptation in populations of the copepod Eurytemora affinis spanning natural salinity and temperature gradients in the Baltic and North Seas. Based on whole-genome sequencing of 11 populations, we found population genomic signatures of selection associated with salinity and temperature gradients in both seas, indicating local adaptation, with ‘ion transmembrane transport’ as the most enriched gene ontology category under selection. Interestingly, the single nucleotide polymorphisms (SNPs) associated with responses to salinity and temperature were uncorrelated. We found clear population structure between the Baltic and North Seas, along with signals of admixture between populations, consistent with the presence of gene flow both within and between the seas. Our results suggest that gene flow of beneficial alleles from across the environmental gradients could provide the genetic substrate for populations to adapt to future climate change.

Saline migrants into freshwater habitats constitute among the most destructive invaders in aquatic ecosystems throughout the globe. However, evolutionary and physiological mechanisms underlying such habitat transitions remain poorly understood. To explore mechanisms of freshwater adaptation and distinguish between adaptive (evolutionary) and acclimatory (plastic) responses to salinity change, we examined genome-wide patterns of gene expression between ancestral saline and derived freshwater populations of the Eurytemora affinis species complex, reared under two different common-garden conditions (0 vs. 15 PSU). We found that evolutionary shifts in gene expression (between saline and freshwater inbred lines) showed far greater changes and were more widespread than acclimatory responses to salinity (0 vs. 15 PSU). Most notably, many genes showing evolutionary shifts in gene expression across the salinity boundary were associated with ion transport function, with inorganic cation transmembrane transport forming the largest Gene Ontology category. Of particular interest was the sodium transporter, the Na+/H+ antiporter (NHA) gene family, which was discovered in animals relatively recently. A few key ion regulatory genes, such as NHA paralog #7, demonstrated concordant evolutionary and plastic shifts in gene expression, suggesting the evolution of ion transporter plasticity and function during rapid invasions into novel salinities. Moreover, freshwater invasions were associated with the evolution of reduced plasticity in the freshwater population, again for the same key ion transporters, consistent with the predicted evolution of canalization following adaptation to stressful conditions. Our results have important implications for understanding invasion mechanisms by some of the most widespread invaders in aquatic habitats.