How fast are viruses spreading in the wild?

Genomic data collected from viral outbreaks can be exploited to reconstruct the dispersal history of viral lineages in a two-dimensional space using continuous phylogeographic inference. These spatially explicit reconstructions can subsequently be used to estimate dispersal metrics allowing to unveil the dispersal dynamics and evaluate the capacity to spread among hosts. Heterogeneous sampling intensity of genomic sequences can however impact the accuracy of dispersal insights gained through phylogeographic inference. In our study, we implement a simulation framework to evaluate the robustness of three dispersal metrics - a lineage dispersal velocity, a diffusion coefficient, and an isolation-by-distance signal metric - to the sampling effort. Our results reveal that both the diffusion coefficient and isolation-by-distance signal metrics appear to be robust to the number of samples considered for the phylogeographic reconstruction. We then use these two dispersal metrics to compare the dispersal pattern and capacity of various viruses spreading in animal populations. Our comparative analysis reveals a broad range of isolation-by-distance patterns and diffusion coefficients mostly reflecting the dispersal capacity of the main infected host species but also, in some cases, the likely signature of rapid and/or long-distance dispersal events driven by human-mediated movements through animal trade. Overall, our study provides key recommendations for the lineage dispersal metrics to consider in future studies and illustrates their application to compare the spread of viruses in various settings.

Revisiting the origins of the Sobemovirus genus: A case for ancient origins of plant viruses.

The discrepancy between short- and long-term rate estimates, known as the time-dependent rate phenomenon (TDRP), poses a challenge to extrapolating evolutionary rates over time and reconstructing evolutionary history of viruses. The TDRP reveals a decline in evolutionary rate estimates with the measurement timescale, explained empirically by a power-law rate decay, notably observed in animal and human viruses. A mechanistic evolutionary model, the Prisoner of War (PoW) model, has been proposed to address TDRP in viruses. Although TDRP has been studied in animal viruses, its impact on plant virus evolutionary history remains largely unexplored. Here, we investigated the consequences of TDRP in plant viruses by applying the PoW model to reconstruct the evolutionary history of sobemoviruses, plant pathogens with significant importance due to their impact on agriculture and plant health. Our analysis showed that the Sobemovirus genus dates back over four million years, indicating an ancient origin. We found evidence that supports deep host jumps to Poaceae, Fabaceae, and Solanaceae occurring between tens to hundreds of thousand years ago, followed by specialization. Remarkably, the TDRP-corrected evolutionary history of sobemoviruses was extended far beyond previous estimates that had suggested their emergence nearly 9,000 years ago, a time coinciding with the Neolithic period in the Near East. By incorporating sequences collected through metagenomic analyses, the resulting phylogenetic tree showcases increased genetic diversity, reflecting a deep history of sobemovirus species. We identified major radiation events beginning between 4,600 to 2,000 years ago, which aligns with the Neolithic period in various regions, suggesting a period of rapid diversification from then to the present. Our findings make a case for the possibility of deep evolutionary origins of plant viruses.

Genetic diversity and epidemic histories of rice yellow mottle virus in Ghana.

Rice yellow mottle virus (RYMV) has persisted as a major biotic constraint to rice production in Africa. However, no data on RYMV epidemics were available in Ghana, although it is an intensive rice-producing country. Surveys were performed from 2010 to 2020 in eleven rice-growing regions of Ghana. Symptom observations and serological detections confirmed that RYMV is circulating in most of these regions. Coat protein gene and complete genome sequencings revealed that RYMV in Ghana almost exclusively belongs to the strain S2, one of the strains covering the largest area in West Africa. We also detected the presence of the S1ca strain which is being reported for the first time outside its area of origin. These results suggested a complex epidemiological history of RYMV in Ghana and a recent expansion of S1ca to West Africa. Phylogeographic analyses reconstructed at least five independent RYMV introductions in Ghana for the last 40 years, probably due to rice cultivation intensification in West Africa leading to a better circulation of RYMV. In addition to identifying some routes of RYMV dispersion in Ghana, this study contributes to the epidemiological surveillance of RYMV and helps to design disease management strategies, especially through breeding for rice disease resistance.

ICTV Virus Taxonomy Profile: Solemoviridae 2021.

The family Solemoviridae includes viruses with icosahedral particles (26-34 nm in diameter) assembled on T=3 symmetry with a 4-6 kb positive-sense, monopartite, polycistronic RNA genome. Transmission of members of the genera Sobemovirus and Polemovirus occurs via mechanical wounding, vegetative propagation, insect vectors or abiotically through soil; members of the genera Polerovirus and Enamovirus are transmitted by specific aphids. Most solemoviruses have a narrow host range. This is a summary of the International Committee on Taxonomy of Viruses (ICTV) Report on the family Solemoviridae, which is available at ictv.global/report/solemoviridae.

EvoLaps: a web interface to visualize continuous phylogeographic reconstructions.

BACKGROUND: Phylogeographic reconstructions serve as a basis to understand the spread and evolution of pathogens. Visualization of these reconstructions often lead to complex graphical representations which are difficult to interpret. RESULT: We present EvoLaps, a user-friendly web interface to visualize phylogeographic reconstructions based on the analysis of latitude/longitude coordinates with various clustering levels. EvoLaps also produces transition diagrams that provide concise and easy to interpret summaries of phylogeographic reconstructions. CONCLUSION: The main contribution of EvoLaps is to assemble known numerical and graphical methods/tools into a user-friendly interface dedicated to the visualization and edition of evolutionary scenarios based on continuous phylogeographic reconstructions. EvoLaps is freely usable at www.evolaps.org .

Rivers and landscape ecology of a plant virus, Rice yellow mottle virus along the Niger Valley.

To investigate the spread of Rice yellow mottle virus (RYMV) along the Niger River, regular sampling of virus isolates was conducted along 500 km of the Niger Valley in the Republic of Niger and was complemented by additional sampling in neighbouring countries in West Africa and Central Africa. The spread of RYMV into and within the Republic of Niger was inferred as a continuous process using a Bayesian statistical framework applied previously to reconstruct its dispersal history in West Africa, East Africa, and Madagascar. The spatial resolution along this section of the Niger River was the highest implemented for RYMV and possibly for any plant virus. We benefited from the results of early field surveys of the disease for the validation of the phylogeographic reconstruction and from the well-documented history of rice cultivation changes along the Niger River for their interpretation. As a prerequisite, the temporal signal of the RYMV data sets was revisited in the light of recent methodological advances. The role of the hydrographic network of the Niger Basin in RYMV spread was examined, and the link between virus population dynamics and the extent of irrigated rice was assessed. RYMV was introduced along the Niger River in the Republic of Niger in the early 1980s from areas to the southwest of the country where rice was increasingly grown. Viral spread was triggered by a major irrigation scheme made of a set of rice perimeters along the river valley. The subsequent spatial and temporal host continuity and the inoculum build-up allowed for a rapid spread of RYMV along the Niger River, upstream and downstream, over hundreds of kilometres, and led to the development of severe epidemics. There was no evidence of long-distance dissemination of the virus through natural water. Floating rice in the main meanders of the Middle Niger did not contribute to virus dispersal from West Africa to Central Africa. RYMV along the Niger River is an insightful example of how agricultural intensification favours pathogen emergence and spread.

Comparing patterns and scales of plant virus phylogeography: Rice yellow mottle virus in Madagascar and in continental Africa.

Rice yellow mottle virus (RYMV) in Madagascar Island provides an opportunity to study the spread of a plant virus disease after a relatively recent introduction in a large and isolated country with a heterogeneous host landscape ecology. Here, we take advantage of field survey data on the occurrence of RYMV disease throughout Madagascar dating back to the 1970s, and of virus genetic data from ninety-four isolates collected since 1989 in most regions of the country to reconstruct the epidemic history. We find that the Malagasy isolates belong to a unique recombinant strain that most likely entered Madagascar through a long-distance introduction from the most eastern part of mainland Africa. We infer the spread of RYMV as a continuous process using a Bayesian statistical framework. In order to calibrate the time scale in calendar time units in this analysis, we pool the information about the RYMV evolutionary rate from several geographical partitions. Whereas the field surveys and the phylogeographic reconstructions both point to a rapid southward invasion across hundreds of kilometers throughout Madagascar within three to four decades, they differ on the inferred origin location and time of the epidemic. The phylogeographic reconstructions suggest a lineage displacement and unveil a re-invasion of the northern regions that may have remained unnoticed otherwise. Despite ecological differences that could affect the transmission potential of RYMV in Madagascar and in mainland Africa, we estimate similar invasion and dispersal rates. We could not identify environmental factors that have a relevant impact on the lineage dispersal velocity of RYMV in Madagascar. This study highlights the value and complementarity of (historical) nongenetic and (more contemporaneous) genetic surveillance data for reconstructing the history of spread of plant viruses.

Complete Genome Sequences of Rice Yellow Mottle Virus Isolates from the Federal Democratic Republic of Ethiopia.

The full-length genomes of two isolates of Rice yellow mottle virus from Ethiopia were sequenced. A comparison with 28 sequences from East Africa showed that they clustered within a new strain named S4et, related to the S4mg and S4ug strains found in the Lake Victoria Basin and Madagascar, respectively.

On the importance of negative controls in viral landscape phylogeography.

Phylogeographic reconstructions are becoming an established procedure to evaluate the factors that could impact virus spread. While a discrete phylogeographic approach can be used to test predictors of transition rates among discrete locations, alternative continuous phylogeographic reconstructions can also be exploited to investigate the impact of underlying environmental layers on the dispersal velocity of a virus. The two approaches are complementary tools for studying pathogens' spread, but in both cases, care must be taken to avoid misinterpretations. Here, we analyse rice yellow mottle virus (RYMV) sequence data from West and East Africa to illustrate how both approaches can be used to study the impact of environmental factors on the virus' dispersal frequency and velocity. While it was previously reported that host connectivity was a major determinant of RYMV spread, we show that this was a false positive result due to the lack of appropriate negative controls. We also discuss and compare the phylodynamic tools currently available for investigating the impact of environmental factors on virus spread.

Full-Length Genome Sequences of Recombinant and Nonrecombinant Sympatric Strains of Rice yellow mottle virus from Western Kenya.

Five isolates of Rice yellow mottle virus from western Kenya were fully sequenced. One isolate of strain S4lv had been collected in 1966. Two isolates belonged to the emerging strain S4ug recently described in Uganda. Two isolates collected in 2012 are putative recombinants between the S4lv and S4ug strains.

Identification of a Hypervirulent Pathotype of Rice yellow mottle virus: A Threat to Genetic Resistance Deployment in West-Central Africa.

Rice yellow mottle virus (RYMV) causes high losses to rice production in Africa. Several sources of varietal high resistance are available but the emergence of virulent pathotypes that are able to overcome one or two resistance alleles can sometimes occur. Both resistance spectra and viral adaptability have to be taken into account to develop sustainable rice breeding strategies against RYMV. In this study, we extended previous resistance spectrum analyses by testing the rymv1-4 and rymv1-5 alleles that are carried by the rice accessions Tog5438 and Tog5674, respectively, against isolates that are representative of RYMV genetic and pathogenic diversity. Our study revealed a hypervirulent pathotype, named thereafter pathotype T', that is able to overcome all known sources of high resistance. This pathotype, which is spatially localized in West-Central Africa, appears to be more abundant than previously suspected. To better understand the adaptive processes of pathotype T', molecular determinants of resistance breakdown were identified via Sanger sequencing and validated through directed mutagenesis of an infectious clone. These analyses confirmed the key role of convergent nonsynonymous substitutions in the central part of the viral genome-linked protein to overcome RYMV1-mediated resistance. In addition, deep-sequencing analyses revealed that resistance breakdown does not always coincide with fixed mutations. Actually, virulence mutations that are present in a small proportion of the virus population can be sufficient for resistance breakdown. Considering the spatial distribution of RYMV strains in Africa and their ability to overcome the RYMV resistance genes and alleles, we established a resistance-breaking risk map to optimize strategies for the deployment of sustainable and resistant rice lines in Africa.

Complete Genome Sequence of a New Strain of Rice yellow mottle virus from Malawi, Characterized by a Recombinant VPg Protein.

The complete sequence of the isolate Mw10 of Rice yellow mottle virus was determined. Sequence comparisons revealed 8.4% to 10.7% nucleotide divergence from the published sequences, resulting in the definition of the strain S7. Importantly, a putative recombination event was identified encompassing the viral genome-linked protein involved in host adaptation.

Emergence of rice yellow mottle virus in eastern Uganda: Recent and singular interplay between strains in East Africa and in Madagascar.

Epidemics of rice yellow mottle virus (RYMV) have developed recently in eastern Uganda, close to Lake Victoria in East Africa. Unexpectedly, all isolates from the affected area belonged to a single strain (named S4ug), a strain that is different from the S4lv strain that has been prevalent in the Lake Victoria basin for the past five decades. Interestingly, the S4ug strain is most closely related at the genomic level (except ORF1) to the strain present in Madagascar (S4mg), 2000km away. The minor parent of the S4mg recombinant strain could not be detected. Molecular clock dating analysis indicated that the singular sequence of events - that associated the emergence of a new strain (S4ug), a modular recombination between closely related strains (S4mg and S4ug) and a long distance transmission (S4mg) - occurred recently, within the past few decades. This finding is at variance with the process of gradual strain dispersal and diversification over two centuries throughout Africa that was previously established.

The biogeography of viral emergence: rice yellow mottle virus as a case study.

Rice yellow mottle virus (RYMV) exemplifies the key role in plant virus emergence of the early steps of crop extension and intensification in traditional agriculture. In East Africa, RYMV emerged in the 19(th) century after rice intensification along the Indian Ocean coast, and later spread inland concomitantly with rice introduction. In West Africa, the contrasted history of rice cultivation among regions differently shaped RYMV populations. A biogeographical approach - which jointly considers the spatial distribution of the virus and its hosts over time - was applied to reach these conclusions. We linked the evolution of RYMV over the past two centuries to a geographical map of the history of rice cultivation in Africa.

Host ecology determines the dispersal patterns of a plant virus.

Since its isolation in 1966 in Kenya, rice yellow mottle virus (RYMV) has been reported throughout Africa resulting in one of the economically most important tropical plant emerging diseases. A thorough understanding of RYMV evolution and dispersal is critical to manage viral spread in tropical areas that heavily rely on agriculture for subsistence. Phylogenetic analyses have suggested a relatively recent expansion, perhaps driven by the intensification of agricultural practices, but this has not yet been examined in a coherent statistical framework. To gain insight into the historical spread of RYMV within Africa rice cultivations, we analyse a dataset of 300 coat protein gene sequences, sampled from East to West Africa over a 46-year period, using Bayesian evolutionary inference. Spatiotemporal reconstructions date the origin of RMYV back to 1852 (1791-1903) and confirm Tanzania as the most likely geographic origin. Following a single long-distance transmission event from East to West Africa, separate viral populations have been maintained for about a century. To identify the factors that shaped the RYMV distribution, we apply a generalised linear model (GLM) extension of discrete phylogenetic diffusion and provide strong support for distances measured on a rice connectivity landscape as the major determinant of RYMV spread. Phylogeographic estimates in continuous space further complement this by demonstrating more pronounced expansion dynamics in West Africa that are consistent with agricultural intensification and extensification. Taken together, our principled phylogeographic inference approach shows for the first time that host ecology dynamics have shaped the historical spread of a plant virus.

Cassava Ivorian bacilliform virus is a member of the genus Anulavirus.

The complete genomic sequence of Cassava Ivorian bacilliform virus (CIBV) is described. The virus has a genomic organization similar to that of pelargonium zonate spot virus (PZSV), the type member of the genus Anulavirus, but it is most closely related to a second, recently described, anulavirus, Amazon lily mild mottle virus (ALiMMV).

Alternative mutational pathways, outside the VPg, of rice yellow mottle virus to overcome eIF(iso)4G-mediated rice resistance under strong genetic constraints.

The adaptation of rice yellow mottle virus (RYMV) to rymv1-mediated resistance has been reported to involve mutations in the viral genome-linked protein (VPg). In this study, we analysed several cases of rymv1-2 resistance breakdown by an isolate with low adaptability. Surprisingly, in these rarely occurring resistance-breaking (RB) genotypes, mutations were detected outside the VPg, in the ORF2a/ORF2b overlapping region. The causal role of three mutations associated with rymv1-2 resistance breakdown was validated via directed mutagenesis of an infectious clone. In resistant plants, these mutations increased viral accumulation as efficiently as suboptimal RB mutations in the VPg. Interestingly, these mutations are located in a highly conserved, but unfolded, domain. Altogether, our results indicate that under strong genetic constraints, a priori unfit genotypes can follow alternative mutational pathways, i.e. outside the VPg, to overcome rymv1-2 resistance.

Sites under positive selection modulate the RNA silencing suppressor activity of rice yellow mottle virus movement protein P1.

RNA silencing is a eukaryotic mechanism for RNA-based gene regulation that plays an essential role in diverse biological processes, such as defence against viral infections. The P1 of rice yellow mottle virus (RYMV) is a movement protein and displays RNA silencing suppression activity with variable efficiency, depending on the origin of the isolates. In this study, the positive selection pressure acting on the P1 protein gene was assessed. A site-by-site analysis of the dN/dS ratio was performed and 18 positively selected sites were identified. Four of these were mutated, and the ability to suppress RNA silencing was evaluated for the resulting mutants in a transient expression assay. All mutations affected quantitatively RNA silencing suppression, one caused a significant decrease in the activity and three significantly increased it. This work demonstrates, for what is to the best of our knowledge the first time, that the RYMV gene encoding the P1 RNA silencing suppressor is under adaptive evolution.

Rice yellow mottle virus in Madagascar and in the Zanzibar Archipelago; island systems and evolutionary time scale to study virus emergence.

Rice yellow mottle virus (RYMV), of the genus Sobemovirus, is a major threat to rice cultivation in Africa. Long range transmission of RYMV, difficult to study experimentally, is inferred from a detailed analysis of the molecular diversity of the virus in Madagascar and in the Zanzibar Archipelago (Zanzibar and Pemba Islands; Tanzania) compared with that found elsewhere in Africa. A unique successful introduction of RYMV to Madagascar, which is ca. 400 km from mainland Africa, contrasted with recurrent introductions of the virus to the Zanzibar Archipelago, ca. 40 km from the East African coast. Accordingly, RYMV dispersal over distances of hundreds of kilometers is rare whereas spread of the virus over distances of tens of kilometers is relatively frequent. The dates of introduction of RYMV to Madagascar and to Pemba Island were estimated from three sets of ORF4 sequences of virus isolates collected between 1966 and 2011. They were compared with the dates of the first field detection in Madagascar (1989) and in Pemba Island (1990). The estimates did not depend substantially on the data set used or on the evolutionary model applied and their credible intervals were narrow. The estimated dates are recent - 1978 (1969-1986) and 1985 (1977-1993) in Madagascar and in Pemba Island, respectively - compared to the early diversification of RYMV in East Africa ca. 200 years ago. They predated by 5-10 years the first field detections in these islands. The interplay between virus sources, rice cultivation and long range dispersal which led to RYMV emergence and spread is enlightened.

The origin and evolutionary history of HIV-1 subtype C in Senegal.

BACKGROUND: The classification of HIV-1 strains in subtypes and Circulating Recombinant Forms (CRFs) has helped in tracking the course of the HIV pandemic. In Senegal, which is located at the tip of West Africa, CRF02_AG predominates in the general population and Female Sex Workers (FSWs). In contrast, 40% of Men having Sex with Men (MSM) in Senegal are infected with subtype C. In this study we analyzed the geographical origins and introduction dates of HIV-1 C in Senegal in order to better understand the evolutionary history of this subtype, which predominates today in the MSM population METHODOLOGY/PRINCIPAL FINDINGS: We used a combination of phylogenetic analyses and a Bayesian coalescent-based approach, to study the phylogenetic relationships in pol of 56 subtype C isolates from Senegal with 3,025 subtype C strains that were sampled worldwide. Our analysis shows a significantly well supported cluster which contains all subtype C strains that circulate among MSM in Senegal. The MSM cluster and other strains from Senegal are widely dispersed among the different subclusters of African HIV-1 C strains, suggesting multiple introductions of subtype C in Senegal from many different southern and east African countries. More detailed analyses show that HIV-1 C strains from MSM are more closely related to those from southern Africa. The estimated date of the MRCA of subtype C in the MSM population in Senegal is estimated to be in the early 80's. CONCLUSIONS/SIGNIFICANCE: Our evolutionary reconstructions suggest that multiple subtype C viruses with a common ancestor originating in the early 1970s entered Senegal. There was only one efficient spread in the MSM population, which most likely resulted from a single introduction, underlining the importance of high-risk behavior in spread of viruses.