Host replacement dynamics shape virulence and genome evolution in a plant RNA virus

Abstract We have investigated how the dynamics of host replacement affect the evolution of a plant RNA virus. Specifically, we have examined how sudden vs. gradual transitions from more susceptible to less susceptible Arabidopsis thaliana genotypes influence turnip mosaic virus’ virulence and population genomic diversity. Our results show that the evolution of virulence and the complexity of the mutant swarm is linked to both the type of host succession and the genetic basis of the host resistance. Faster changes in virulence are observed after sudden transitions, with an evolutionary trend towards more severe symptoms that appear later during infection. Gradual transitions resulted in greater population mutational richness and higher genetic polymorphism compared to sudden transitions. In contrast, beneficial mutations associated with sudden transitions had stronger fitness effects than those linked to gradual transitions. This research highlights the importance of considering the rate of environmental changes in virus evolution and provides insights into predicting how viruses adapt and evolve in temporally changing environments, with implications for agriculture and public health.