Predation drove adaptive metabolomic evolution
By measuring the metabolomes of three subpopulations separated in time that belong to one continuous population and underwent strong changes in fish predation pressure, we could directly demonstrate rapid metabolomic evolution within a single natural population. The three D. magnasubpopulations differed in their ‘metabolic fingerprint’ not only in the presence (Figure S3) but also in the absence (Figure S4) of fish kairomones, suggesting rapid evolution of constitutive metabolic differences in this population. Besides constitutive evolution, we also observed rapid evolution of plastic metabolomic responses to predation risk. These patterns complement the rapid constitutive evolution and evolution of plastic responses to predation risk in life history, morphology and behaviour in this study system (Stoks et al.2016). We have poor knowledge on whether and how the metabolome evolves in natural populations. As a notable exception, the marine snailLittorina littorea evolved different metabolomic responses to ocean acidification at much longer timescales associated with postglacial range expansion, which was linked to regional adaptation in physiology and life history (Calosi et al. 2017).
Two lines of evidence suggest that the rapid evolution of metabolomic responses to predation risk was adaptive. First, the high-fish subpopulation showed a stronger metabolomic response to fish kairomones compared to the pre-fish and reduced-fish subpopulations. This was illustrated both by the high-fish subpopulation having the most metabolites responsive to fish kairomones and the largest magnitude of the multivariate metabolomic reaction norm in response to fish kairomones. Second, in line with fish predators being only present in the high-fish and reduced-fish periods (Cousyn et al. 2001), these two subpopulations had a more similar direction of the multivariate metabolomic response under predation compared to the pre-fish subpopulation. Also this pattern is consistent with the multivariate reaction norms for life history, behaviour and morphology (Stoks et al. 2016). Notably, the metabolomic responses to fish kairomones in the reduced-fish subpopulation did not fully convert back to those of the pre-fish subpopulation, similar to what was observed for life history traits in earlier work (Stoks et al. 2016). This illustrates also at the metabolomic level that evolution in response to a new selective factor is not necessarily fully reversed when that selection factor is relaxed (Lahti et al. 2009).