Predicting the First Steps of Evolution in Randomly Assembled Microbial Communities

Microbial communities can self-assemble into highly diverse states with predictable community-level phenotypes. However, the residents of these communities can rapidly evolve over time by acquiring additional mutations in their genomes. When a mutant invades a population, it competes for ecological niches both with its parent strain and with the other strains in the surrounding community. This complex interplay between ecology and evolution is difficult to capture with existing community assembly theory. Here, we introduce a replica-theoretic approach for predicting the first steps of evolution in randomly assembled communities that compete for substitutable resources. We show how the invasion fitness of a mutant and the probability that it coexists with its parent depends on the size of the community, the saturation of its niches, and the metabolic overlap between its members. We find that successful mutations are often able to coexist with their parent strains, even in saturated communities with low niche availability. This coexistence probability increases further when the mutations impose a cost on the maximum growth rate. These results suggest that even small amounts of evolution can produce microbial communities with multiple coexisting strains of the same species.