Dissecting the transcriptomic basis of phenotypic evolution in an aquatic keystone grazer

Abstract

Cultural eutrophication is one of the largest threats to aquatic ecosystems with devastating ecological and economic consequences. Although Daphnia, a keystone grazer crustacean, can mitigate some negative effects of eutrophication in freshwater habitats, it is itself affected by changes in nutrient composition. Previous studies have shown evolutionary adaptation of Daphnia to environmental change, including high phosphorus levels. While phosphorus is an essential macronutrient, it negatively affects Daphnia life history when present in excessive concentrations. Here, we map weighted gene co-expression networks to phosphorus-related phenotypic traits in centuries-old ancestral Daphnia and their modern descendants, contrasting pre- and post-eutrophication environments. We find that evolutionary fine-tuning of transcriptional responses is manifested at a basic (cellular) phenotypic level, and is strongly correlated to an evolved plasticity of gene expression. At a higher phenotypic level, this contributes to the maintenance of physiological homeostasis, and a robust preservation of somatic phosphorus concentration.