Host-parasite coevolution promotes innovation through deformations in fitness landscapes

During the struggle for survival, populations occasionally evolve new functions that give them access to untapped ecological opportunities. Theory suggests that coevolution between species can promote the evolution of such innovations by deforming fitness landscapes in ways that open new adaptive pathways. We directly tested this idea by using high throughput gene editing-phenotyping technology (MAGE-Seq) to measure the fitness landscape of a virus, bacteriophage λ, as it coevolved with its host, the bacterium Escherichia coli. Through computer simulations of λ’s evolution on the empirical fitness landscape, we showed that λ was more likely to evolve to use a new receptor if it experienced a shift in its fitness landscape caused by coevolution. Detailed examination of a single coevolving laboratory population showed that the first mutation λ evolved required the presence of the ancestral host, whereas later steps in λ’s evolution required the shift to a resistant host. When replays of the coevolution experiment were run with an intervention that disrupted coevolution, λ did not evolve to use OmpF. This study provides direct evidence for the role of coevolution in driving evolutionary novelty and provides a quantitative framework for predicting evolution in coevolving ecological communities.