Time-Sampled Population Sequencing Reveals the Interplay of Selection and Genetic Drift in Experimental Evolution of Potato Virus Y

Abstract

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 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.

Transmission modes affect the population structure of potato virus Y in potato

“…Combined with novel and evolving bioinformatics algorithms, HTS has improved our ability to study the processes that shape viral populations within hosts with an unprecedented level of genetic resolution [18][19][20].…”

“…Nevertheless, technological challenges in measuring the complete genetic variation in a virus population have been lessened by the advent of high-throughput sequencing (HTS) technology, which allows detection of viral mutations at very low frequencies [ 17 ]. Combined with novel and evolving bioinformatics algorithms, HTS has improved our ability to study the processes that shape viral populations within hosts with an unprecedented level of genetic resolution [ 18 – 20 ].…”

Next Generation Sequencing for Detection and Discovery of Plant Viruses and Viroids: Comparison of Two Approaches

“…Also, de novo assembly of longer viral contigs could be complicated due to short reads lengths (Boonham et al, 2014 ; Roossinck et al, 2015 ; Adams and Fox, 2016 ). On the other hand, the approach is very generic, using the same protocol of sample preparation for many different plant species and doesn't require high quality of RNA input (Kutnjak et al, 2017 ).…”

Experimental evolution for niche breadth in bacteriophage T4 highlights the importance of structural genes

“…Many of these studies have focused on virus systems and experimental exposure to different (or new) hosts, as the type, range, and availability of hosts present in the environment is an important source of selection pressure (Cooper & Scott, 2001; Crill, Wichman, & Bull, 2000; S. Duffy, Burch, & Turner, 2007; Kutnjak, Elena, & Ravnikar, 2017; Morley, Mendiola, & Turner, 2015; Ogbunugafor et al 2013, Novella et al, 1995). This and other experimental work in this realm has provided varying levels of support for the tradeoff hypothesis, indicating that there are still gaps in our knowledge regarding how viruses respond to changes in their environment (Bedhomme, Lafforgue, & Elena, 2012; Novella, Hershey, Escarmis, Domingo, & Holland, 1999; Turner & Elena, 2000).…”