Evolutionary rescue and adaptive reversal allowed the persistence of freshwater copepods during historical lake acidification and pH recovery

The persistence of populations facing severe environmental disturbance can be enabled by natural selection on heritable phenotypic variation – a process known as evolutionary rescue. Examples of evolutionary rescue have been documented in wild populations. Still, few studies have investigated the combination of factors (demographic, genetic, and environmental) that facilitate the rescue of populations in complex natural settings. This is important because the interplay of these factors in wild populations can cause uncertainty about the long-term outcome of evolutionary rescue: the persistence of rescued populations could potentially be threatened during environmental recovery due to a loss of genetic diversity from strong selection and demographic effects and reduced fitness in the recovered environment. Here, we used copepod resting eggs of Leptodiaptomus minutus from three time periods of lake ecological history, spanning ≈200 generations in two populations impacted by historical acidification. Whole genome sequencing of the resting eggs allowed us to uncover allele frequency shifts associated with the acidification followed by pH recovery. We used a resurrection ecology approach to retrace adaptive shifts concomitant with environmental transitions. Resurrected copepods from the pre-acidification period showed sensitivity to acidity, while individuals from the acidification period were adapted to acidic pH and showed high fitness overall. This tolerance was subsequently lost during pH recovery. We found evidence of rapid directional selection in genome scans, consistent with the results of the phenotypic assays. Significant changes in allele frequencies of outlier loci during acidification were followed by a reversal in the recovered populations, implying that the loss of acid tolerance could be due to an adaptive reversal. Demographic models indicated a demographic decline during the acidification process followed by population recovery, suggesting that selection led to evolutionary rescue. By employing temporal genomic data and resurrection ecology experiments in lake ecosystems that have been impacted by historical human disturbance, this study fills a critical knowledge gap about the long-term implications of evolutionary rescue in the wild.