Avoiding dead ends: the experimental evolution of constraint as adaptation to environmental variation

Environmental unpredictability can result in the evolution of bet-hedging traits, which maximize long-term fitness but are, by definition, suboptimal over short time scales. However, because suboptimal traits are expected to be purged by selection under benign 'background' environments over the shorter term, the persistence of bet hedging over the longer time scales at which they are adaptive remains perplexing. Here, we propose and test the hypothesis that bet hedging to strong but rare events persists through the evolution of constraints on short-term adaptation to benign environments. To test this hypothesis, we experimentally evolve initially thermotolerant strains of Saccharomyces cerevisiae across sequential treatment regimes in which the frequency of extreme heat shocks decreases. The constraint hypothesis predicts that lines evolved under severe but comparatively rare heat shocks will have become more 'selection proof' to benign conditions. As predicted, evolution under severe but low-frequency heat shocks resulted in constrained adaptation to short-term benign conditions. This result suggests that evolutionary constraint can be adaptive and provides a proof-of-concept solution to the apparent paradox that the evolution of bet hedging requires maladaptation. Whether there are limits to the evolution of constraint as adaptation to stochasticity over longer time scales remains an open question.