Resurrecting the metabolome: rapid evolution magnifies the metabolomic plasticity to predation in a natural Daphnia population

Populations rely on already present plastic responses (ancestral plasticity) and evolution (including both evolution of mean trait values, constitutive evolution, and evolution of plasticity) to adapt to novel environmental conditions. Because of the lack of evidence from natural populations, controversy remains regarding the interplay between ancestral plasticity and rapid evolution in driving responses to new stressors. We addressed this topic at the level of the metabolome utilizing a resurrected natural population of the water flea Daphnia magna that underwent a human-caused increase followed by a reduction in predation pressure within ~16 years. Predation risk induced plastic changes in the metabolome which were mainly related to shifts in amino acid and sugar metabolism, suggesting predation risk affected protein and sugar utilization to increase energy supply. Both the constitutive and plastic components of the metabolic profiles showed rapid, probably adaptive evolution whereby ancestral plasticity and evolution contributed nearly equally to the total changes of the metabolomes. The subpopulation that experienced the strongest fish predation pressure and showed the strongest phenotypic response, also showed the strongest metabolomic response to fish kairomones, both in terms of the number of responsive metabolites and in the amplitude of the multivariate metabolomic reaction norm. More importantly, the metabolites with higher ancestral plasticity showed stronger evolution of plasticity when predation pressure increased, while this pattern reversed when predation pressure relaxed. Our results therefore highlight that the evolution in response to a novel pressure in a natural population magnified the metabolomic plasticity to this stressor.