Physiological constrains underlying history-dependent fitness effects in fluctuating environments

Environmental change is ubiquitous in natural settings, requiring organisms to adapt across multiple environments. Our previous work has shown that environmental fluctuations pose the novel challenge of adaptation to rapid environmental transitions in a collection of experimental evolution S. cerevisiae mutants. In contrast to experimental evolution, which proceeds via a small number of large-effect mutations, natural variation encompasses many genomic changes accumulated over long timescales. Whether findings from lab-based evolution experiments generalize to natural variants remains an open question. Here, we ask how environmental fluctuations affect the fitness of a collection of ~350 DNA-barcoded natural S. cerevisiaeisolates across ~15 environments. We observe history-dependence as large differences between fitness in fluctuating environments and expected fitness from static environments. Furthermore, fitness change in one component of a fluctuating environment is negatively correlated with fitness change in the other component, representing a trade-off in history-dependent effects. Additionally, we find that a resource-allocation based dynamical system model recapitulates our observations. The agreement between experimental results in two different collections of strains and our model suggests a general physiological constraint underlying the effects of environmental fluctuations on fitness.