Award: OCE-1658517

Global climate change poses catastrophic threats to biodiversity and ecosystem integrity of the planet. Rising global temperatures are projected to result in widespread local extinctions, species range shifts, and disruption of food webs. One of the most devastating consequences of climate change is the change in ocean salinity. In high-latitude coastal regions, increases in precipitation and ice melt are causing salinity declines on unprecedented rapid rates. Most aquatic life is adapted to a narrow range of salinities, such that even a small change in salinity could be devastating. The objective of this project was to explore the ability to adapt in response to salinity change by a widespread estuarine zooplankton, the copepod Eurytemora affinis species complex. This copepod is a dominant plankton species in coastal habitats and serves as a very important food source for major fisheries, such as salmon, herring, and anchovy. When the rate of environmental change is faster than the ability to acclimate, a population often must evolve to avoid extinction. Given the pressing need to determine the evolutionary responses to climate change, the goals of this project were to address the following questions: (1) To what extent and how fast could populations evolve in response to rapid salinity and temperature changes? (2) What are the genetic mechanisms that allow populations evolve to a rapidly changing environment? To address these questions, this study analyzed the evolutionary responses of populations of the E. affinis species complex to the impacts of salinity (and temperature). We performed population genomic surveys of wild populations and natural selection experiments in the laboratory. We conducted population genomic surveys of E. affinis populations along salinity and temperature gradients in the St. Lawrence drainage system, Gulf of Mexico, and the Baltic Sea. Additionally, we imposed laboratory natural selection on populations of E. affinis collected from the Baltic Sea. We sequenced the populations before, during, and after imposing laboratory selection to determine the rate of evolutionary change and the trajectory of alleles under selection. Natural selection experiments (experimental evolution) constitute powerful tools for determining the rate, trajectory, and limits of adaptation. We found exceptional parallelism, with natural selection acting on the same alleles (genetic variants) during independent salinity transitions. We made the important discovery that the alleles under parallel selection were already present in the native range populations (under balancing selection). Interestingly, the genomic regions under natural selection during salinity change were heavily enriched with ion transporter genes, which likely aids in taking up ions from freshwater environments. A key novel finding of this study is that a genetic mechanism called "positive epistasis" could drive rapid parallel adaptation (evolution) in the face of rapid environmental change, such as climate change. Positive epistasis is the case when the positive effect of an allele (variant of a gene) is increased by the presence of other alleles at other genes in the genome (i.e., positive gene-gene interactions). That is, the fitness of an individual copepod will be greater if it has a very specific combination of alleles at different genes. Our results suggest that positive fitness effects of the combination of alleles (positive epistasis) could drive the same sets of alleles to be repeatedly favored by natural selection (resulting in parallel evolution). These results suggest that particular sets of ion transporter paralogs form co-adapted gene complexes that cooperate in function and evolve together in response to environmental change. Thus, our results indicate that specific beneficial alleles are necessary for adaptation to a novel freshwater environment. Moreover, a very specific combination of those alleles appears to be favored by natural selection during salinity adaptation (positive epistasis). In addition, these alleles need to be present in the starting population, so that natural selection can favor those beneficial alleles in the novel habitat. Our study revealed very specific conditions that are required for adaptation to occur, giving us the power to assess the potential of populations to evolve in response to rapid environmental change. Many populations will not satisfy these requirements and are likely to go extinct. The potential for evolutionary adaptation in estuarine species is critically important for projecting the future sustainability of food web integrity and coastal fisheries. Estuaries and adjacent coastal waters serve a multitude of essential ecosystem functions and support major fisheries worldwide. The economic value of estuarine fisheries amounts to hundreds of billions of dollars in the US alone. The copepod E. affinis complex has been studied extensively as a commercially important species for fisheries (e.g. salmon, herring, haddock). Even a modest change of ~20% in copepod production could have millions of dollars in impact on fish harvests. We have gained important insights from this study on what is required for populations to evolve in response to climate variables. Most notably, we have uncovered some key mechanisms that enable rapid adaptation to occur. Last Modified: 07/03/2022 Submitted by: Carol E Lee