Species interactions constrain adaptation and preserve ecological stability in an experimental microbial community.

Species loss within a microbial community can increase resource availability and spur adaptive evolution. Environmental shifts that cause species loss or fluctuations in community composition are expected to become more common, so it is important to understand the evolutionary forces that shape the stability and function of the emergent community. Here we study experimental cultures of a simple, ecologically stable community of Saccharomyces cerevisiae and Lactobacillus plantarum, in order to understand how the presence or absence of a species impacts coexistence over evolutionary timescales. We found that evolution in coculture led to drastically altered evolutionary outcomes for L. plantarum, but not S. cerevisiae. Both monoculture- and co-culture-evolved L. plantarum evolved dozens of mutations over 925 generations of evolution, but only L. plantarum that had evolved in isolation from S. cerevisiae lost the capacity to coexist with S. cerevisiae. We find that the evolutionary loss of ecological stability corresponds with fitness differences between monoculture-evolved L. plantarum and S. cerevisiae and genetic changes that repeatedly evolve across the replicate populations of L. plantarum. This work shows how coevolution within a community can prevent destabilising evolution in individual species, thereby preserving ecological diversity and stability, despite rapid adaptation.

The evolution of coexistence from competition in experimental co-cultures of Escherichia coli and Saccharomyces cerevisiae.

Microbial communities are comprised of many species that coexist on small spatial scales. This is difficult to explain because many interspecies interactions are competitive, and ecological theory predicts that one species will drive the extinction of another species that competes for the same resource. Conversely, evolutionary theory proposes that natural selection can lead to coexistence by driving competing species to use non-overlapping resources. However, evolutionary escape from extinction may be slow compared to the rate of competitive exclusion. Here, we use experimental co-cultures of Escherichia coli and Saccharomyces cerevisiae to study the evolution of coexistence in species that compete for resources. We find that while E. coli usually outcompetes S. cerevisiae in co-culture, a few populations evolved stable coexistence after ~1000 generations of coevolution. We sequenced S. cerevisiae and E. coli populations, identified multi-hit genes, and engineered alleles from these genes into several genetic backgrounds, finding that some mutations modified interactions between E. coli and S. cerevisiae. Together, our data demonstrate that coexistence can evolve, de novo, from intense competition between two species with no history of coevolution.