Resurrection genomics provides molecular and phenotypic evidence of rapid adaptation to salinization in a keystone aquatic species

Abstract

Ecologists and evolutionary biologists are increasingly cognizant of rapid adaptation in wild populations. Rapid adaptation to anthropogenic environmental change is critical for maintaining biodiversity and ecosystems services into the future. Anthropogenic salinization of freshwater ecosystems is quickly emerging as a primary threat, which is well documented in the northern temperate ecoregion. Specifically, many northern temperate lakes have undergone extensive salinization because of urbanization and the associated increase in impervious surfaces causing runoff, and the extensive use of road deicing salts (e.g., NaCl). It remains unclear if increasing salinization will lead to extirpation of species from these systems. Using a "resurrection genomics" approach, we investigated whether the keystone aquatic herbivore, Daphnia pulicaria, has evolved increased salinity tolerance in a severely salinized lake located in Minnesota, USA. Whole genome resequencing of 54 Daphnia clones from the lake and hatched from resting eggs that represent a 25-year temporal contrast demonstrates that many regions of the genome containing genes related to osmoregulation are under selection in the study population. Tolerance assays of clones revealed that the most recent clones are more tolerant to salinity than older clones; this pattern is concomitant with the temporal pattern of stabilizing salinity in this lake. Together, our results demonstrate that keystone species such as Daphnia can rapidly adapt to increasing freshwater salinization. Further, our results indicate that rapid adaptation to salinity may allow lake Daphnia populations to persist in the face of anthropogenic salinization maintaining the food webs and ecosystem services they support despite global environmental change. Significance StatementRapid adaptation to human-induced environmental change is critical for preserving biodiversity and ecosystem services into the future. A key question is whether populations of keystone species can rapidly adapt to maintain the ecosystems they support. We investigated rapid adaptation to anthropogenic salinization in Daphnia pulicaria, a keystone aquatic herbivore in lake ecosystems. By resuscitating decades-old resting eggs, we investigate genomic changes across an approximately 25-year temporal contrast from a severely salinized lake. We report that the genes showing signatures of natural selection throughout the genome are related to osmoregulation and ion regulation. Phenotyping clones for salinity tolerance revealed evidence that genetic changes may underlie rapid evolution. We provide molecular genomic and phenotypic evidence for rapid adaptation to salinity in D. pulicaria.