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.