Rapid Evolution in a Fluctuating Environment

Organisms experience many different environments over their evolutionary histories, shaping the suite of mutations that successfully reach fixation. The influence of a changing environment is especially relevant in microbes, whose rapid reproduction drives evolution on timescales comparable to fluctuations in the abiotic environment. However, predicting evolutionary outcomes in large microbial populations is difficult because beneficial mutations on different genetic backgrounds — and with different environmental preferences — must compete to avoid extinction. Here, we resolve this difficulty by developing a theoretical approach to predict the fixation probability of a mutation as a function of its fitness in each environment, the rate of adaptation of its competitors, and the timescale of environmental fluctuation. We find that even when their average fitness effect is the same, mutations with an environment-dependent fitness effect can be exponentially more likely to reach fixation than mutations insensitive to environmental change. When environment-sensitive mutations are common, the most successful lineages tend to accumulate mutations in tandem with environmental changes, resulting in a suite of "compensatory'' mutations with opposing environmental tradeoffs. These results provide a vital baseline for experiments analyzing evolution in fluctuating environments, and highlight that a variety of outcomes are possible depending on the timescales involved.