Abstract
ABSTRACTRNA viruses are one of the fastest-evolving biological entities. Within their hosts, they exist as genetically diverse populations (i.e., viral mutant swarms), which are sculpted by different evolutionary mechanisms, such as mutation, natural selection, and genetic drift, and also the interactions between genetic variants within the mutant swarms. To elucidate the mechanisms that modulate the population diversity of an important plant-pathogenic virus, we performed evolution experiments with Potato virus Y (PVY) in potato genotypes that differ in their defense response against the virus. Using deep sequencing of small RNAs, we followed the temporal dynamics of standing and newly generated variations in the evolving viral lineages. A time-sampled approach allowed us to (i) reconstruct theoretical haplotypes in the starting population by using clustering of single nucleotide polymorphisms' trajectories and (ii) use quantitative population genetics approaches to estimate the contribution of selection and genetic drift, and their interplay, to the evolution of the virus. We detected imprints of strong selective sweeps and narrow genetic bottlenecks, followed by the shift in frequency of selected haplotypes. Comparison of patterns of viral evolution in differently susceptible host genotypes indicated possible diversifying evolution of PVY in the less-susceptible host (efficient in the accumulation of salicylic acid).IMPORTANCE High diversity of within-host populations of RNA viruses is an important aspect of their biology, since they represent a reservoir of genetic variants, which can enable quick adaptation of viruses to a changing environment. This study focuses on an important plant virus, Potato virus Y, and describes, at high resolution, temporal changes in the structure of viral populations within different potato genotypes. A novel and easy-to-implement computational approach was established to cluster single nucleotide polymorphisms into viral haplotypes from very short sequencing reads. During the experiment, a shift in the frequency of selected viral haplotypes was observed after a narrow genetic bottleneck, indicating an important role of the genetic drift in the evolution of the virus. On the other hand, a possible case of diversifying selection of the virus was observed in less susceptible host genotypes.
Highlights
RNA viruses are one of the fastest-evolving biological entities
Virus titers approached a plateau in all three genotypes 21 dpi, the time point at which sampling for virus population sequencing was performed
Following the general trends of Potato virus Y (PVY) evolution in the experiment, a narrow genetic bottleneck in one of the passages was detected, coinciding with the shift in the selected virus haplotypes in many lineages, indicating the power of genetic drift to change the location of a virus population in the fitness landscape
Summary
RNA viruses are one of the fastest-evolving biological entities. Within their hosts, they exist as genetically diverse populations (i.e., viral mutant swarms), which are sculpted by different evolutionary mechanisms, such as mutation, natural selection, and genetic drift, and the interactions between genetic variants within the mutant swarms. Fast replication, coupled with high mutation and recombination rates [3,4,5] and large populations, enables RNA viruses to quickly adapt to changing environments These properties render them interesting for studies of basic evolutionary processes, e.g., mutation, selection, and genetic drift. Host switches can represent important ecological changes, posing different, and sometimes conflicting, selection pressures on the virus population [8] These selective forces can leave an imprint in the viral genomes, which can show parallel fixed mutations in viral lineages independently evolved into the same host species [9, 10]. Evidence for host specific convergent mutations were shown during the experimental evolution of Tobacco etch virus (TEV) in different ecotypes of the same species [17]
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