To realize the rapid responses to new environmental stressors, populations may rely not only on initial plastic responses (i.e. ancestral plasticity) but also on rapid evolutionary changes, whereby the latter can involve both evolution of mean trait values (i.e., constitutive evolution) and evolution of plasticity. Against this background, important outstanding questions in current evolutionary biology are what the relative contributions of the plastic and evolutionary responses are and how these relate to each other in determining rates of rapid adaptation. Here, we studied these questions at the level of metabolomics by quantifying the plastic and evolutionary responses of the metabolome in a resurrected natural population of the water flea Daphnia magna. This population underwent a strong increase followed by a strong reduction in predation pressure within ~16 years. Changes of metabolic profiles were analyzed by different multivariate analyses. We partitioned the total changes of metabolomic profiles to quantify the relative contributions of ancestral plasticity, constitutive evolution, and evolution of plasticity. Finally, we explored whether and how plastic responses and evolutionary responses covaried with each other.
Results/Conclusions
Predation risk significantly changed the metabolomes which were mainly related to shifts in amino acid and sugar metabolism, indicating predation risk affected protein utilization and energy supply. Both the constitutive and plastic components of the metabolic profiles showed rapid evolution. Ancestral plasticity and evolutionary responses contributed nearly equally to the total changes of the metabolomes during both transitions in fish predation. The high-fish subpopulation that experienced the strongest fish predation pressure 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. These patterns matched previously documented adaptive patterns in life history, morphology and behavioural traits in this study system, suggesting adaptive evolution of the metabolomic responses. The metabolites with higher ancestral plasticity showed stronger evolution of plasticity as well as of total evolution when the predation pressure increased, while this pattern reversed when the predation pressure relaxed, indicating adaptive evolution in response to predation in this resurrected population magnified the plastic response of the metabolome to this stressor. These analyses enabled us to get unique insights in the rapid evolution of the metabolome in a natural population in response to a novel stressor.