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While many freshwater invaders originate from saline habitats, the physiological mechanisms involved are poorly understood. We investigated the evolution of ion transporter Na+/K+-ATPase (NKA) protein expression between ancestral saline and freshwater invading populations of the copepod Eurytemora carolleae (Atlantic clade of the E. affinis complex). We compared in situ NKA expression between populations under common-garden conditions at three salinities in the maxillary glands. We found the evolution of reduced NKA expression in the freshwater population under freshwater conditions and reduced plasticity (canalization) across salinities, relative to the saline population. Our results support the hypothesis that maxillary glands are involved in ion reabsorption from excretory fluids at low-salinity conditions in the saline population. However, mechanisms of freshwater adaptation, such as increased ion uptake from the environment, might reduce the need for ion reabsorption in the freshwater population. These patterns of ion transporter expression contribute insights into the evolution of ionic regulation during habitat change. 

Abstract 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 copepod Eurytemora 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. 

Abstract 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. 

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.