Estimating virus effective population size and selection without neutral markers

Rousseau, Elsa; Moury, Benoît; Mailleret, Ludovic; Senoussi, Rachid; Palloix, Alain; Simon, Vincent; Valière, Sophie; Grognard, Frédéric; Fabre, Frédéric

doi:10.1371/journal.ppat.1006702

Cited by 21 publications

(44 citation statements)

References 56 publications

(77 reference statements)

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“…However, we detected selection for specific variants of the markers that we used for both the N and S segments during our experiments. We thus adapted a recently developed statistical method (24) to jointly estimate selection coefficients (s) and N e ( Table 1). The results revealed selection in favor of the mys2 over the mys7 marker for segment N and in favor of the mys8 over the mys1 marker for segment S. The statistical analysis also showed that the N e values of the N and S segments of FBNSV were small, varying from Table 1).…”

Section: Resultsmentioning

confidence: 99%

Small Bottleneck Size in a Highly Multipartite Virus during a Complete Infection Cycle

Gallet

Fabre

Thébaud

et al. 2018

J Virol

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Multipartite viruses package their genomic segments independently and thus incur the risk of being unable to transmit their entire genome during host-to-host transmission if they undergo severe bottlenecks. In this paper, we estimated the bottleneck size during one infection cycle of (FBNSV), an octopartite nanovirus whose segments have been previously shown to converge to particular and unequal relative frequencies within host plants and aphid vectors. Two methods were used to derive this estimate, one based on the probability of transmission of the virus and the other based on the temporal evolution of the relative frequency of markers for two genomic segments, one frequent and one rare (segment N and S, respectively), both in plants and vectors. Our results show that FBNSV undergoes severe bottlenecks during aphid transmission. Further, even though the bottlenecks are always narrow under our experimental conditions, they slightly widen with the number of transmitting aphids. In particular, when several aphids are used for transmission, the bottleneck size of the segments is also affected by within-plant processes and, importantly, significantly differs across segments. These results indicate that genetic drift not only must be an important process affecting the evolution of these viruses but also that these effects vary across genomic segments and, thus, across viral genes, a rather unique and intriguing situation. We further discuss the potential consequences of our findings for the transmission of multipartite viruses. Multipartite viruses package their genomic segments in independent capsids. The most obvious cost of such genomic structure is the risk of losing at least one segment during host-to-host transmission. A theoretical study has shown that for nanoviruses, composed of 6 to 8 segments, hundreds of copies of each segment need to be transmitted to ensure that at least one copy of each segment was present in the host. These estimations seem to be very high compared to the size of the bottlenecks measured with other viruses. Here, we estimated the bottleneck size during one infection cycle of FBNSV, an octopartite nanovirus. We show that these bottlenecks are always narrow (few viral particles) and slightly widen with the number of transmitting aphids. These results contrast with theoretical predictions and illustrate the fact that a new conceptual framework is probably needed to understand the transmission of highly multipartite viruses.

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Section: Resultsmentioning

confidence: 99%

Small Bottleneck Size in a Highly Multipartite Virus during a Complete Infection Cycle

Gallet

Fabre

Thébaud

et al. 2018

J Virol

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“…These describe features of gene populations, using mathematical models, and compare observed features with those likely to result from sequential random changes. Popgen analyses have been used to study potyvirus populations within plant populations (e.g., Achon [64]; Li et al [65]; Wang et al [66]; Hajizadeh et al [67]) and, increasingly, virus populations within individual plants (e.g., Cuevas et al [68]; Domingo and Perales [69]; Dunham et al [70]; Kutnjak et al [71]; Rousseau et al [72]; Seo et al [73]). Such studies have shown that the effective populations of potyviruses are all around 10,000 [74], and the "The high potential for genetic variation in plant viruses need not necessarily result in high diversity of virus populations.…”

Section: Population Geneticsmentioning

confidence: 99%

The Potyviruses: An Evolutionary Synthesis Is Emerging

Gibbs

Hajizadeh

Ohshima

et al. 2020

Viruses

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In this review, encouraged by the dictum of Theodosius Dobzhansky that “Nothing in biology makes sense except in the light of evolution”, we outline the likely evolutionary pathways that have resulted in the observed similarities and differences of the extant molecules, biology, distribution, etc. of the potyvirids and, especially, its largest genus, the potyviruses. The potyvirids are a family of plant-infecting RNA-genome viruses. They had a single polyphyletic origin, and all share at least three of their genes (i.e., the helicase region of their CI protein, the RdRp region of their NIb protein and their coat protein) with other viruses which are otherwise unrelated. Potyvirids fall into 11 genera of which the potyviruses, the largest, include more than 150 distinct viruses found worldwide. The first potyvirus probably originated 15,000–30,000 years ago, in a Eurasian grass host, by acquiring crucial changes to its coat protein and HC-Pro protein, which enabled it to be transmitted by migrating host-seeking aphids. All potyviruses are aphid-borne and, in nature, infect discreet sets of monocotyledonous or eudicotyledonous angiosperms. All potyvirus genomes are under negative selection; the HC-Pro, CP, Nia, and NIb genes are most strongly selected, and the PIPO gene least, but there are overriding virus specific differences; for example, all turnip mosaic virus genes are more strongly conserved than those of potato virus Y. Estimates of dN/dS (ω) indicate whether potyvirus populations have been evolving as one or more subpopulations and could be used to help define species boundaries. Recombinants are common in many potyvirus populations (20%–64% in five examined), but recombination seems to be an uncommon speciation mechanism as, of 149 distinct potyviruses, only two were clear recombinants. Human activities, especially trade and farming, have fostered and spread both potyviruses and their aphid vectors throughout the world, especially over the past five centuries. The world distribution of potyviruses, especially those found on islands, indicates that potyviruses may be more frequently or effectively transmitted by seed than experimental tests suggest. Only two meta-genomic potyviruses have been recorded from animal samples, and both are probably contaminants.

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“…through the measurement of temporal changes in allele frequencies has remained a major focus of population genetics since the founding of the field (Fisher 1930;Wright 1931). Advancements in sequencing technologies over the last decade have dramatically increased the availability of genomewide time-sampled polymorphism data for a wide variety of organisms, and several methods have been developed to analyze such data (Malaspinas et al 2012;Mathieson and McVean 2013;Foll et al 2014a;Lacerda and Seoighe 2014;Steinrücken et al 2014;Ferrer-Admetlla et al 2016;Schraiber et al 2016;Shim et al 2016;Rousseau et al 2017). Of primary interest is the estimation of site-specific selection coefficients, and new methods account for nonequilibrium demography and environmental fluctuations by, for example, accounting for effective population size, population structure, and changing selection intensities.…”

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confidence: 99%

Inferring Demography and Selection in Organisms Characterized by Skewed Offspring Distributions

Sackman

Harris²,

Jensen³

2019

Genetics

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The recent increase in time-series population genomic data from experimental, natural, and ancient populations has been accompanied by a promising growth in methodologies for inferring demographic and selective parameters from such data. However, these methods have largely presumed that the populations of interest are well-described by the Kingman coalescent. In reality, many groups of organisms, including viruses, marine organisms, and some plants, protists, and fungi, typified by high variance in progeny number, may be best characterized by multiple-merger coalescent models. Estimation of population genetic parameters under Wright-Fisher assumptions for these organisms may thus be prone to serious mis-inference. We propose a novel method for the joint inference of demography and selection under the C-coalescent model, termed Multiple-Merger Coalescent Approximate Bayesian Computation, or MMC-ABC. We first demonstrate mis-inference under the Kingman, and then exhibit the superior performance of MMC-ABC under conditions of skewed offspring distributions. In order to highlight the utility of this approach, we reanalyzed previously published drug-selection lines of influenza A virus. We jointly inferred the extent of progeny-skew inherent to viral replication and identified putative drug-resistance mutations.

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Estimating virus effective population size and selection without neutral markers

Cited by 21 publications

References 56 publications

Small Bottleneck Size in a Highly Multipartite Virus during a Complete Infection Cycle

Small Bottleneck Size in a Highly Multipartite Virus during a Complete Infection Cycle

The Potyviruses: An Evolutionary Synthesis Is Emerging

Inferring Demography and Selection in Organisms Characterized by Skewed Offspring Distributions

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