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

Research output: Contribution to journalArticlepeer-review

Authors

  • Chao Zhang
  • Lynn Govaert
  • Luc De Meester
  • Robby Stoks

Colleges, School and Institutes

External organisations

  • Shandong University
  • Katholieke Universiteit Leuven
  • Swiss Federal Institute of Aquatic Science and Technology

Abstract

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.

Bibliographic note

Funding Information: Financial support came from National Natural Science Foundation of China (42007229), China Postdoctoral Science Foundation (2019M662337), Post‐doctoral Innovation Research Program of Shandong Province (236346), Research Grants from FWO Flanders (G.0943.15), and the KU Leuven Research Fund (C16/17/002). We thank Dr Ralf Weber and Dr Gavin Lloyd for helping with the metabolomic data analysis. Publisher Copyright: © 2021 John Wiley & Sons Ltd

Details

Original languageEnglish
Pages (from-to)2285-2297
Number of pages13
JournalMolecular Ecology
Volume30
Issue number10
Early online date15 Mar 2021
Publication statusPublished - May 2021

Keywords

  • adaptation, ancestral plasticity, crustaceans, metabolomics, rapid evolution of metabolic profiles, resurrection ecology