Environmental memory alters the fitness effects of adaptive mutations in fluctuating environments

Abstract

Evolution in a static laboratory environment often proceeds via large-effect beneficial mutations that may become maladaptive in other environments. Conversely, natural settings require populations to endure environmental fluctuations. A sensible assumption is that the fitness of a lineage in a fluctuating environment is the time average of its fitness over the sequence of static conditions it encounters. However, transitions between conditions may pose entirely new challenges, which could cause deviations from this time average. To test this, we tracked hundreds of thousands of barcoded yeast lineages evolving in static and fluctuating conditions and subsequently isolated 900 mutants for pooled fitness assays in 15 environments. Here we find that fitness in fluctuating environments indeed often deviates from the time average, leading to fitness non-additivity. Moreover, closer examination reveals that fitness in one component of a fluctuating environment is often strongly influenced by the previous component. We show that this environmental memory is especially common for mutants with high variance in fitness across tested environments. We use a simple mathematical model and whole-genome sequencing to propose mechanisms underlying this effect, including lag time evolution and sensing mutations. Our results show that environmental fluctuations impact fitness and suggest that variance in static environments can explain these impacts.