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).