Host Abundance and Identity Determine the Epidemiology and Evolution of a Generalist Plant Virus in a Wild Ecosystem

Increasing evidence indicates that in wild ecosystems plant viruses are important ecological agents, and with potential to jump into crops, but only recently have the diversity and population dynamics of wild plant viruses begun to be explored. Theory proposes that biotic factors (e.g., ecosystem biodiversity, host abundance, and host density) and climatic conditions would determine the epidemiology and evolution of wild plant viruses. However, these predictions seldom have been empirically tested. For 3 years, we analyzed the prevalence and genetic diversity of Potyvirus species in preserved riparian forests of Spain. Results indicated that potyviruses were always present in riparian forests, with a novel generalist potyvirus species provisionally named Iberian hop mosaic virus (IbHMV), explaining the largest fraction of infected plants. Focusing on this potyvirus, we analyzed the biotic and climatic factors affecting virus infection risk and population genetic diversity in its native ecosystem. The main predictors of IbHMV infection risk were host relative abundance and species richness. Virus prevalence and host relative abundance were the major factors determining the genetic diversity and selection pressures in the virus population. These observations support theoretical predictions assigning these ecological factors a key role in parasite epidemiology and evolution. Finally, our phylogenetic analysis indicated that the viral population was genetically structured according to host and location of origin, as expected if speciation is largely sympatric. Thus, this work contributes to characterizing viral diversity and provides novel information on the determinants of plant virus epidemiology and evolution in wild ecosystems.