A theoretical framework for how ecological interactions between microbes affect mutant fitness

The distribution of fitness effects (DFE) for spontaneous mutations characterizes both an organ-ism’s evolutionary potential as well as its genomic functions. The DFE of a genome depends on the specific environment in which it is measured, and for microbes a major feature of their environment is the presence of interactions with other species, such as competing for or cross-feeding nutrients. Several recent studies have empirically measured how the DFE of one microbial species changes in the presence of interactions with other species. However, the underlying mechanisms by which this happens, and the statistical patterns they are expected to produce, are unknown. Here we classify two types of statistical changes in the DFE: global changes to the DFE, such as to its mean or variance, and idiosyncratic changes in the fitness of individual mutants, summarized by the correlation of mutant fitness between environments. We first show that both types of effects occur in empirically measured DFEs across a wide range of species and interactions; idiosyncratic effects appear to have a maximum limit and constrain the size of global effects. We then show that a minimal model of an ecological interaction (competition for a single resource) is sufficient to generate both types of effects. Finally, we extend this model to arbitrary quantitative traits to reveal two general mechanisms of how interactions alter the DFE: 1) interactions can globally change fitness by altering the community growth rate, and 2) interactions can idiosyncratically change fitness of individual mutants by altering relative selection on different traits affected by those mutations.