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The role of epistasis in driving adaptation has remained an unresolved problem dating back to the Evolutionary Synthesis. In particular, whether epistatic interactions among genes could promote parallel evolution remains unexplored. To address this problem, we employ an Evolve and Resequence (E&R) experiment, using the copepodEurytemora affinis, to elucidate the evolutionary genomic response to rapid salinity decline. Rapid declines in coastal salinity at high latitudes are a predicted consequence of global climate change. Based on time-resolved pooled whole-genome sequencing, we uncover a remarkably parallel, polygenic response across ten replicate selection lines, with 79.4% of selected alleles shared between lines by the tenth generation of natural selection. Using extensive computer simulations of our experiment conditions, we find that this polygenic parallelism is consistent with positive synergistic epistasis among alleles, far more so than other mechanisms tested. Our study provides experimental and theoretical support for a novel mechanism promoting repeatable polygenic adaptation, a phenomenon that may be common for selection on complex physiological traits.

 

Climate change is causing habitat salinity to transform at unprecedented rates across the globe. While much of the research on climate change has focused on rapid shifts in temperature, far less attention has focused on the effects of changes in environmental salinity. Consequently, predictive studies on the physiological, evolutionary, and migratory responses of organisms and populations to the threats of salinity change are relatively lacking. This omission represents a major oversight, given that salinity is among the most important factors that define biogeographic boundaries in aquatic habitats. In this perspective, we briefly touch on responses of organisms and populations to rapid changes in salinity occurring on contemporary time scales. We then discuss factors that might confer resilience to certain taxa, enabling them to survive rapid salinity shifts. Next, we consider approaches for predicting how geographic distributions will shift in response to salinity change. Finally, we identify additional data that are needed to make better predictions in the future. Future studies on climate change should account for the multiple environmental factors that are rapidly changing, especially habitat salinity.

 

Saline migrants into freshwater habitats constitute among the most destructive invaders in aquatic ecosystems throughout the globe. However, the evolutionary and physiological mechanisms underlying such habitat transitions remain poorly understood. To explore the 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 theEurytemora affinisspecies complex, reared under two different common‐garden conditions (0 versus 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 versus 15 PSU). Most notably, 30–40 genes showing evolutionary shifts in gene expression across the salinity boundary were associated with ion transport function, withinorganic cation transmembrane transportforming 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. Thirty key ion regulatory genes, such as NHA paralogue #7, demonstrated concordant evolutionary and plastic shifts in gene expression, suggesting the evolution of ion transporter function and plasticity 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 evolutionary and physiological mechanisms of range expansions by some of the most widespread invaders in aquatic habitats.

 

Salinity is a key factor that structures biodiversity on the planet. With anthropogenic change, such as climate change and species invasions, many populations are facing rapid and dramatic changes in salinity throughout the globe. Studies on the copepod Eurytemora affinis species complex have implicated ion transporter gene families as major loci contributing to salinity adaptation during freshwater invasions. Laboratory experiments and population genomic surveys of wild populations have revealed evolutionary shifts in genome-wide gene expression and parallel genomic signatures of natural selection during independent salinity transitions. Our results suggest that balancing selection in the native range and epistatic interactions among specific ion transporter paralogs could contribute to parallel freshwater adaptation. Overall, these studies provide unprecedented insights into evolutionary mechanisms underlying physiological adaptation during rapid salinity change.