On the de novo emergence of ecological interactions during evolutionary diversification: A conceptual framework and experimental test

Ecological interactions are crucial to the structure and function of biological communities, but we lack a causal understanding of the forces shaping their emergence during evolutionary diversification. Here we provide a conceptual framework linking different modes of diversification (e.g. ecological diversification), which depend on environmental characteristics, to the evolution of particular interactions (e.g. resource partitioning) in asexual lineages. We tested the framework by examining the net interactions in communities of Pseudomonas aeruginosa produced via experimental evolution in nutritionally simple (SIM) or complex (COM) environments by contrasting the productivity and competitive fitness of whole evolved communities relative to their component isolates. As expected, we found that nutritional complexity drove the evolution of communities with net positive interactions whereas SIM communities had similar performance as their component isolates. A follow-up experiment revealed that high fitness in two COM communities was driven by rare variants (frequency <0.1%) that antagonized PA14, the ancestral strain and common competitor used in fitness assays. Our study suggests that the evolution of de novo ecological interactions in asexual lineages is predictable at a broad scale from environmental conditions. Further, our work demonstrates that rare variants can disproportionately impact the function of relatively simple microbial communities.