Rapid Adaptation through Standing Genetic Variation

A population's or species' ability to survive rapid environmental changes could mitigate global climate change impacts. The problem is that ecologically relevant adaptive change should require many genetic changes to match phenotypes with the new environment. The likelihood of adaptation depends on whether adaptive changes arise from new mutations (hard sweeps) or standing genetic variation (soft sweeps); this is fundamentally important because these different evolutionary processes influence the rate and cost of selection. To examine the different evolutionary processes affecting local adaptation, we examined adaptation in large natural Fundulus heteroclitus populations recently exposed to power station thermal effluents using genotyping-by-sequencing derived single nucleotide polymorphisms (SNPs). Individuals in these locally heated waters have small but significant increase in their thermal tolerance (critical thermal maximum). Similarly, there are significant allele frequency deviations and SNPs with outlier F_ST values: F_ST values that exceed neutral expectations. These patterns reveal that fish living near thermal effluents have rapidly evolved from the standing genetic variation through small allele frequency changes at many loci in a pattern consistent with a soft sweep model of evolution. Furthermore, the adaptive importance of any one locus depends on the acclimation history such that adaptive loci are mutually exclusive to one temperature. Thus, no locus explains variation in thermal tolerance in more than one thermal acclimation environment. These findings suggest that gene-by-environment interactions can contribute to adaptive potential by using standing genetic variation.