Increasing growth temperature alters the within-host competition of viral strains and influences virus genetic variation

Abstract

The emergence of viral diseases in plant crops hamper the sustainability of food production, and this may be boosted by global warming. Concurrently, mixed viral infections are becoming common in plants, of which epidemiology are unpredictable due to within-host virus-virus interactions. However, the extent in which the combined effect of variations in the abiotic components of the plant ecological niche (e.g., temperature) and the prevalence of mixed infections (i.e., within-host interactions among viruses) affect the evolutionary dynamics of viral populations is not well understood. Here, we explore the interplay between ecological and evolutionary factors during viral infections, and show that two individual strains of pepino mosaic virus (PepMV) coexisted in a temperature-dependent continuum between neutral and antagonistic interactions in tomato plants. After a long-term infection, the mutational analysis of the evolved viral genomes revealed strain-specific single-nucleotide polymorphisms that were modulated by the interaction between the type of infection and temperature. Mathematical modeling allowed us to asses a thermal reaction norm for both strains, which indicated that viral replication rates were increased along with increasing temperature in mixed infections, with a remarkable strain-dependent effect. These results suggest that the growth temperature is an ecological driver of virus-virus interactions, with an effect on the genetic diversity of individual viruses co-infecting a host. This research provides insights into the effect that climate change will have on the evolutionary dynamics of viral populations.