Fate of a mutation in a fluctuating environment
Edited by Boris I. Shraiman, University of California, Santa Barbara, CA, and approved July 27, 2015 (received for review March 17, 2015)
Evolution in variable environments depends crucially on the fates of new mutations in the face of fluctuating selection pressures. In constant environments, the relationship between the selective effect of a mutation and the probability that it will eventually fix or go extinct is well understood. However, our understanding of fixation probabilities in fluctuating environmental conditions is limited. Here, we show that temporal fluctuations in environmental conditions can have dramatic effects on the fate of each new mutation, reducing the efficiency of natural selection and increasing the fixation probability of all mutations, including those that are strongly deleterious on average. This makes it difficult for a population to maintain specialist adaptations, even if their benefits outweigh their costs.
Natural environments are never truly constant, but the evolutionary implications of temporally varying selection pressures remain poorly understood. Here we investigate how the fate of a new mutation in a fluctuating environment depends on the dynamics of environmental variation and on the selective pressures in each condition. We find that even when a mutation experiences many environmental epochs before fixing or going extinct, its fate is not necessarily determined by its time-averaged selective effect. Instead, environmental variability reduces the efficiency of selection across a broad parameter regime, rendering selection unable to distinguish between mutations that are substantially beneficial and substantially deleterious on average. Temporal fluctuations can also dramatically increase fixation probabilities, often making the details of these fluctuations more important than the average selection pressures acting on each new mutation. For example, mutations that result in a trade-off between conditions but are strongly deleterious on average can nevertheless be more likely to fix than mutations that are always neutral or beneficial. These effects can have important implications for patterns of molecular evolution in variable environments, and they suggest that it may often be difficult for populations to maintain specialist traits, even when their loss leads to a decline in time-averaged fitness.
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