Genomic adaptation of the water flea Daphnia to elevated temperatures: Insights from power plant-heated lakes

Abstract

Global warming increasingly threatens freshwater biodiversity, highlighting the need to understand how key ecological interactors, such as the zooplankton water flea Daphnia, genetically adapt to rising temperatures. Although local thermal adaptation has been documented in Daphnia, the underlying genomic changes remain poorly resolved. Here, we examined genomes of Daphnia cucullata (a member of the D. longispina complex) from five lakes artificially warmed for six decades by cooling water from power plants (increase of about 2–4°C), and from seven adjacent, control (i.e., unheated) lakes. Heated-lake and unheated-lake populations showed pronounced genomic divergence. Using a Hidden Markov Model framework, we identified highly differentiated genomic intervals (HDGIs) between the two groups, which were significantly enriched near 188 thermal-adaptation candidate genes, supporting a polygenic basis of thermal adaptation. Contrary to previous studies on the D. longispina complex that identified hybridization as a key driver of local adaptation, we found no evidence for adaptive introgression in the heated lakes, despite the presence of D. cucullata × D. galeata hybrids. Adaptive potential, measured as cumulative allelic richness across the set of differentiated loci overlapping or located near thermal adaptation candidate genes, was high across all populations. Strikingly, shifts of formerly rare alleles toward intermediate frequencies have led to a higher genetic diversity at adaptive loci in heated-lake than in unheated-lake populations. Our results identify specific loci associated with thermal adaptation in D. cucullata, demonstrate that adaptation has occurred independently of hybridization, and underscore the importance of standing genetic variation in local populations for adaptive evolution to warming.