Experimental evolution of the host range dynamics in two isolates of potato virus Y

Abstract The emergence of plant viruses is a complex process influenced by viral genetic variation, host species, and environmental factors. To better predict and manage new plant diseases, it is important to understand how viruses adapt to novel hosts. In this study, we examined how two isolates of potato virus Y (PVY), PVYNb and PVYSt, evolve when repeatedly passed through three solanaceous plants: Bentham’s tobacco (Nicotiana benthamiana), potato (Solanum tuberosum), and tomato (Solanum lycopersicum). We also tested whether switching between hosts could reduce the impact of strong population bottlenecks, which often occur in poorly suited hosts. Our findings show that benthamiana supports high viral RNA accumulation and genetically stable diversity, consistent with large effective population sizes. In contrast, potato creates strong bottlenecks, often leading to viral lineage extinction and increased mutation fixation due to genetic drift. Tomato served as an intermediate host, with outcomes varying by virus strain, and acted as a sink host for some lineages, resulting in unsuccessful infection in the next passage. PVYNb showed greater standing diversity and more lineage-specific nonsynonymous change, whereas PVYSt exhibited greater genomic stability and pervasive purifying selection across most cistrons. Only a few late-passage benthamiana lineages displayed elevated πN/πS ratios, indicating that positive selection was rare and not consistently replicated. Overall, our results show that the balance between selection and drift depends strongly on host permissiveness and demographic constraints. Importantly, alternating between permissive and restrictive hosts helped prevent lineage extinction, suggesting that heterogeneous host environments, such as those encountered in agricultural systems, may facilitate virus persistence and adaptation. This study deepens our understanding of the ecological and evolutionary forces that drive the emergence of plant viruses.