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.

Dispersal history of SARS-CoV-2 in Galicia, Spain.

The dynamics of SARS-CoV-2 transmission are influenced by a variety of factors, including social restrictions and the emergence of distinct variants. In this study, we delve into the origins and dissemination of the Alpha, Delta, and Omicron variants of concern in Galicia, northwest Spain. For this, we leveraged genomic data collected by the EPICOVIGAL Consortium and from the GISAID database, along with mobility information from other Spanish regions and foreign countries. Our analysis indicates that initial introductions during the Alpha phase were predominantly from other Spanish regions and France. However, as the pandemic progressed, introductions from Portugal and the USA became increasingly significant. Notably, Galicia's major coastal cities emerged as critical hubs for viral transmission, highlighting their role in sustaining and spreading the virus. This research emphasizes the critical role of regional connectivity in the spread of SARS-CoV-2 and offers essential insights for enhancing public health strategies and surveillance measures.

Genetic insights of H9N2 avian influenza viruses circulating in Mali and phylogeographic patterns in Northern and Western Africa.

Avian influenza viruses (AIVs) of the H9N2 subtype have become widespread in Western Africa since their first detection in 2017 in Burkina Faso. However, the genetic characteristics and diffusion patterns of the H9N2 virus remain poorly understood in Western Africa, mainly due to limited surveillance activities. In addition, Mali, a country considered to play an important role in the epidemiology of AIVs in the region, lacks more comprehensive data on the genetic characteristics of these viruses, especially the H9N2 subtype. To better understand the genetic characteristics and spatio-temporal dynamics of H9N2 virus within this region, we carried out a comprehensive genetic characterization of H9N2 viruses collected through active surveillance in live bird markets in Mali between 2021 and 2022. We also performed a continuous phylogeographic analysis to unravel the dispersal history of H9N2 lineages between Northern and Western Africa. The identified Malian H9N2 virus belonged to the G1 lineage, similar to viruses circulating in both Western and Northern Africa, and possessed multiple molecular markers associated with an increased potential for zoonotic transmission and virulence. Notably, some Malian strains carried the R-S-N-R motif at their cleavage site, mainly observed in H9N2 strains in Asia. Our continuous phylogeographic analysis revealed a single and significant long-distance lineage dispersal event of the H9N2 virus to Western Africa, likely to have originated from Morocco in 2015, shaping the westward diffusion of the H9N2 virus. Our study highlights the need for long-term surveillance of H9N2 viruses in poultry populations in Western Africa, which is crucial for a better understanding of virus evolution and effective management against potential zoonotic AIV strain emergence.

Contribution of climate change to the spatial expansion of West Nile virus in Europe.

West Nile virus (WNV) is an emerging mosquito-borne pathogen in Europe where it represents a new public health threat. While climate change has been cited as a potential driver of its spatial expansion on the continent, a formal evaluation of this causal relationship is lacking. Here, we investigate the extent to which WNV spatial expansion in Europe can be attributed to climate change while accounting for other direct human influences such as land-use and human population changes. To this end, we trained ecological niche models to predict the risk of local WNV circulation leading to human cases to then unravel the isolated effect of climate change by comparing factual simulations to a counterfactual based on the same environmental changes but a counterfactual climate where long-term trends have been removed. Our findings demonstrate a notable increase in the area ecologically suitable for WNV circulation during the period 1901-2019, whereas this area remains largely unchanged in a no-climate-change counterfactual. We show that the drastic increase in the human population at risk of exposure is partly due to historical changes in population density, but that climate change has also been a critical driver behind the heightened risk of WNV circulation in Europe.

Dispersion patterns of SARS-CoV-2 variants Gamma, Lambda and Mu in Latin America and the Caribbean.

Latin America and Caribbean (LAC) regions were an important epicenter of the COVID-19 pandemic and SARS-CoV-2 evolution. Through the COVID-19 Genomic Surveillance Regional Network (COVIGEN), LAC countries produced an important number of genomic sequencing data that made possible an enhanced SARS-CoV-2 genomic surveillance capacity in the Americas, paving the way for characterization of emerging variants and helping to guide the public health response. In this study we analyzed approximately 300,000 SARS-CoV-2 sequences generated between February 2020 and March 2022 by multiple genomic surveillance efforts in LAC and reconstructed the diffusion patterns of the main variants of concern (VOCs) and of interest (VOIs) possibly originated in the Region. Our phylogenetic analysis revealed that the spread of variants Gamma, Lambda and Mu reflects human mobility patterns due to variations of international air passenger transportation and gradual lifting of social distance measures previously implemented in countries. Our results highlight the potential of genetic data to reconstruct viral spread and unveil preferential routes of viral migrations that are shaped by human mobility patterns.

Genomic epidemiology of West Nile virus in Europe.

West Nile virus is one of the most widespread mosquito-borne zoonotic viruses, with unique transmission dynamics in various parts of the world. Genomic surveillance has provided important insights in the global patterns of West Nile virus emergence and spread. In Europe, multiple West Nile virus lineages have been isolated, with lineage 1a and 2 being the main lineages responsible for human infections. In contrast to North America, where a single introduction of lineage 1a resulted in the virus establishing itself in a new continent, at least 13 introductions of lineages 1a and 2 have occurred into Europe, which is likely a vast underestimation of the true number of introductions. Historically, lineage 1a was the main lineage circulating in Europe, but since the emergence of lineage 2 in the early 2000s, the latter has become the predominant lineage. This shift in West Nile virus lineage prevalence has been broadly linked to the expansion of the virus into northerly temperate regions, where autochthonous cases in animals and humans have been reported in Germany and The Netherlands. Here, we discuss how genomic analysis has increased our understanding of the epidemiology of West Nile virus in Europe, and we present a global Nextstrain build consisting of publicly available West Nile virus genomes (https://nextstrain.org/community/grubaughlab/WNV-Global). Our results elucidate recent insights in West Nile virus lineage dynamics in Europe, and discuss how expanded programs can fill current genomic surveillance gaps.

Unravelling the effect of New Year's Eve celebrations on SARS-CoV-2 transmission.

Public holidays have been associated with SARS-CoV-2 incidence surges, although a firm link remains to be established. This association is sometimes attributed to events where transmissions occur at a disproportionately high rate, known as superspreading events. Here, we describe a sudden surge in new cases with the Omicron BA.1 strain amongst higher education students in Belgium. Contact tracers classed most of these cases as likely or possibly infected on New Year's Eve, indicating a direct trigger by New Year celebrations. Using a combination of contact tracing and phylogenetic data, we show the limited role of superspreading events in this surge. Finally, the numerous simultaneous transmissions allowed a unique opportunity to determine the distribution of incubation periods of the Omicron strain. Overall, our results indicate that, even under social restrictions, a surge in transmissibility of SARS-CoV-2 can occur when holiday celebrations result in small social gatherings attended simultaneously and communitywide.

Investigation of an international water polo tournament in Czechia as a potential source for early introduction of the SARS-CoV-2 Omicron variant into Belgium, Switzerland and Germany, November 2021.

BackgroundThe earliest recognised infections by the SARS-CoV-2 Omicron variant (Pango lineage B.1.1.529) in Belgium and Switzerland suggested a connection to an international water polo tournament, held 12-14 November 2021 in Brno, Czechia.AimTo study the arrival and subsequent spread of the Omicron variant in Belgium and Switzerland, and understand the overall importance of this international sporting event on the number of infections in the two countries.MethodsWe performed intensive forward and backward contact tracing in both countries, supplemented by phylogenetic investigations using virus sequences of the suspected infection chain archived in public databases.ResultsThrough contact tracing, we identified two and one infected athletes of the Belgian and Swiss water polo teams, respectively, and subsequently also three athletes from Germany. In Belgium and Switzerland, four and three secondary infections, and three and one confirmed tertiary infections were identified. Phylogenetic investigation demonstrated that this sporting event played a role as the source of infection, but without a direct link with infections from South Africa and not as a superspreading event; the virus was found to already be circulating at that time in the countries involved.ConclusionThe SARS-CoV-2 Omicron variant started to circulate in Europe several weeks before its identification in South Africa on 24 November 2021. Accordingly, it can be assumed that travel restrictions are usually implemented too late to prevent the spread of newly detected SARS-CoV-2 variants to other regions. Phylogenetic analysis may modify the perception of an apparently clear result of intensive contact tracing.

The International Virus Bioinformatics Meeting 2023.

The 2023 International Virus Bioinformatics Meeting was held in Valencia, Spain, from 24-26 May 2023, attracting approximately 180 participants worldwide. The primary objective of the conference was to establish a dynamic scientific environment conducive to discussion, collaboration, and the generation of novel research ideas. As the first in-person event following the SARS-CoV-2 pandemic, the meeting facilitated highly interactive exchanges among attendees. It served as a pivotal gathering for gaining insights into the current status of virus bioinformatics research and engaging with leading researchers and emerging scientists. The event comprised eight invited talks, 19 contributed talks, and 74 poster presentations across eleven sessions spanning three days. Topics covered included machine learning, bacteriophages, virus discovery, virus classification, virus visualization, viral infection, viromics, molecular epidemiology, phylodynamic analysis, RNA viruses, viral sequence analysis, viral surveillance, and metagenomics. This report provides rewritten abstracts of the presentations, a summary of the key research findings, and highlights shared during the meeting.

Complete genome reconstruction of the global and European regional dispersal history of the lumpy skin disease virus.

IMPORTANCE: Lumpy skin disease virus (LSDV) has a complex epidemiology involving multiple strains, recombination, and vaccination. Its DNA genome provides limited genetic variation to trace outbreaks in space and time. Sequencing of LSDV whole genomes has also been patchy at global and regional scales. Here, we provide the first fine-grained whole genome sequence sampling of a constrained LSDV outbreak (southeastern Europe, 2015-2017), which we analyze along with global publicly available genomes. We formally evaluate the past occurrence of recombination events as well as the temporal signal that is required for calibrating molecular clock models and subsequently conduct a time-calibrated spatially explicit phylogeographic reconstruction. Our study further illustrates the importance of accounting for recombination events before reconstructing global and regional dynamics of DNA viruses. More LSDV whole genomes from endemic areas are needed to obtain a comprehensive understanding of global LSDV dispersal dynamics.

Dispersal history and bidirectional human-fish host switching of invasive, hypervirulent Streptococcus agalactiae sequence type 283.

Human group B Streptococcus (GBS) infections attributable to an invasive, hypervirulent sequence type (ST) 283 have been associated with freshwater fish consumption in Asia. The origin, geographic dispersion pathways and host transitions of GBS ST283 remain unresolved. We gather 328 ST283 isolate whole-genome sequences collected from humans and fish between 1998 and 2021, representing eleven countries across four continents. We apply Bayesian phylogeographic analyses to reconstruct the dispersal history of ST283 and combine ST283 phylogenies with genetic markers and host association to investigate host switching and the gain and loss of antimicrobial resistance and virulence factor genes. Initial dispersal within Asia followed ST283 emergence in the early 1980s, with Singapore, Thailand and Hong Kong observed as early transmission hubs. Subsequent intercontinental dispersal originating from Vietnam began in the decade commencing 2001, demonstrating ST283 holds potential to expand geographically. Furthermore, we observe bidirectional host switching, with the detection of more frequent human-to-fish than fish-to-human transitions, suggesting that sound wastewater management, hygiene and sanitation may help to interrupt chains of transmission between hosts. We also show that antimicrobial resistance and virulence factor genes were lost more frequently than gained across the evolutionary history of ST283. Our findings highlight the need for enhanced surveillance, clinical awareness, and targeted risk mitigation to limit transmission and reduce the impact of an emerging pathogen associated with a high-growth aquaculture industry.

Genomic monitoring of SARS-CoV-2 variants using sentinel SARI hospital surveillance.

Background: To support the COVID-19 pandemic response, many countries, including Belgium, implemented baseline genomic surveillance (BGS) programs aiming to early detect and characterize new SARS-CoV-2 variants. In parallel, Belgium maintained a sentinel network of six hospitals that samples patients with severe acute respiratory infections (SARI) and integrated SARS-CoV-2 detection within a broader range of respiratory pathogens. We evaluate the ability of the SARI surveillance to monitor general trends and early signals of viral genetic evolution of SARS-CoV-2 and compare it with the BGS as a reference model. Methods: Nine-hundred twenty-five SARS-CoV-2 positive samples from patients fulfilling the Belgian SARI definition between January 2020 and December 2022 were sequenced using the ARTIC Network amplicon tiling approach on a MinION platform. Weekly variant of concern (VOC) proportions and types were compared to those that were circulating between 2021 and 2022, using 96,251 sequences of the BGS. Results: SARI surveillance allowed timely detection of the Omicron (BA.1, BA.2, BA.4, and BA.5) and Delta (B.1.617.2) VOCs, with no to 2 weeks delay according to the start of their epidemic growth in the Belgian population. First detection of VOCs B.1.351 and P.1 took longer, but these remained minor in Belgium. Omicron BA.3 was never detected in SARI surveillance. Timeliness could not be evaluated for B.1.1.7, being already major at the start of the study period. Conclusions: Genomic surveillance of SARS-CoV-2 using SARI sentinel surveillance has proven to accurately reflect VOCs detected in the population and provides a cost-effective solution for long-term genomic monitoring of circulating respiratory viruses.

Projected decline in European bumblebee populations in the twenty-first century.

Habitat degradation and climate change are globally acting as pivotal drivers of wildlife collapse, with mounting evidence that this erosion of biodiversity will accelerate in the following decades1-3. Here, we quantify the past, present and future ecological suitability of Europe for bumblebees, a threatened group of pollinators ranked among the highest contributors to crop production value in the northern hemisphere4-8. We demonstrate coherent declines of bumblebee populations since 1900 over most of Europe and identify future large-scale range contractions and species extirpations under all future climate and land use change scenarios. Around 38-76% of studied European bumblebee species currently classified as 'Least Concern' are projected to undergo losses of at least 30% of ecologically suitable territory by 2061-2080 compared to 2000-2014. All scenarios highlight that parts of Scandinavia will become potential refugia for European bumblebees; it is however uncertain whether these areas will remain clear of additional anthropogenic stressors not accounted for in present models. Our results underline the critical role of global change mitigation policies as effective levers to protect bumblebees from manmade transformation of the biosphere.

Uncovering the endemic circulation of rabies in Cambodia.

In epidemiology, endemicity characterizes sustained pathogen circulation in a geographical area, which involves a circulation that is not being maintained by external introductions. Because it could potentially shape the design of public health interventions, there is an interest in fully uncovering the endemic pattern of a disease. Here, we use a phylogeographic approach to investigate the endemic signature of rabies virus (RABV) circulation in Cambodia. Cambodia is located in one of the most affected regions by rabies in the world, but RABV circulation between and within Southeast Asian countries remains understudied. Our analyses are based on a new comprehensive data set of 199 RABV genomes collected between 2014 and 2017 as well as previously published Southeast Asian RABV sequences. We show that most Cambodian sequences belong to a distinct clade that has been circulating almost exclusively in Cambodia. Our results thus point towards rabies circulation in Cambodia that does not rely on external introductions. We further characterize within-Cambodia RABV circulation by estimating lineage dispersal metrics that appear to be similar to other settings, and by performing landscape phylogeographic analyses to investigate environmental factors impacting the dispersal dynamic of viral lineages. The latter analyses do not lead to the identification of environmental variables that would be associated with the heterogeneity of viral lineage dispersal velocities, which calls for a better understanding of local dog ecology and further investigations of the potential drivers of RABV spread in the region. Overall, our study illustrates how phylogeographic investigations can be performed to assess and characterize viral endemicity in a context of relatively limited data.

The recency and geographical origins of the bat viruses ancestral to SARS-CoV and SARS-CoV-2.

The emergence of SARS-CoV in 2002 and SARS-CoV-2 in 2019 has led to increased sampling of related sarbecoviruses circulating primarily in horseshoe bats. These viruses undergo frequent recombination and exhibit spatial structuring across Asia. Employing recombination-aware phylogenetic inference on bat sarbecoviruses, we find that the closest-inferred bat virus ancestors of SARS-CoV and SARS-CoV-2 existed just ~1-3 years prior to their emergence in humans. Phylogeographic analyses examining the movement of related sarbecoviruses demonstrate that they traveled at similar rates to their horseshoe bat hosts and have been circulating for thousands of years in Asia. The closest-inferred bat virus ancestor of SARS-CoV likely circulated in western China, and that of SARS-CoV-2 likely circulated in a region comprising southwest China and northern Laos, both a substantial distance from where they emerged. This distance and recency indicate that the direct ancestors of SARS-CoV and SARS-CoV-2 could not have reached their respective sites of emergence via the bat reservoir alone. Our recombination-aware dating and phylogeographic analyses reveal a more accurate inference of evolutionary history than performing only whole-genome or single gene analyses. These results can guide future sampling efforts and demonstrate that viral genomic fragments extremely closely related to SARS-CoV and SARS-CoV-2 were circulating in horseshoe bats, confirming their importance as the reservoir species for SARS viruses.

Comparing the evolutionary dynamics of predominant SARS-CoV-2 virus lineages co-circulating in Mexico.

Over 200 different SARS-CoV-2 lineages have been observed in Mexico by November 2021. To investigate lineage replacement dynamics, we applied a phylodynamic approach and explored the evolutionary trajectories of five dominant lineages that circulated during the first year of local transmission. For most lineages, peaks in sampling frequencies coincided with different epidemiological waves of infection in Mexico. Lineages B.1.1.222 and B.1.1.519 exhibited similar dynamics, constituting clades that likely originated in Mexico and persisted for >12 months. Lineages B.1.1.7, P.1 and B.1.617.2 also displayed similar dynamics, characterized by multiple introduction events leading to a few successful extended local transmission chains that persisted for several months. For the largest B.1.617.2 clades, we further explored viral lineage movements across Mexico. Many clades were located within the south region of the country, suggesting that this area played a key role in the spread of SARS-CoV-2 in Mexico.

Genomic assessment of invasion dynamics of SARS-CoV-2 Omicron BA.1.

Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) variants of concern (VOCs) now arise in the context of heterogeneous human connectivity and population immunity. Through a large-scale phylodynamic analysis of 115,622 Omicron BA.1 genomes, we identified >6,000 introductions of the antigenically distinct VOC into England and analyzed their local transmission and dispersal history. We find that six of the eight largest English Omicron lineages were already transmitting when Omicron was first reported in southern Africa (22 November 2021). Multiple datasets show that importation of Omicron continued despite subsequent restrictions on travel from southern Africa as a result of export from well-connected secondary locations. Initiation and dispersal of Omicron transmission lineages in England was a two-stage process that can be explained by models of the country's human geography and hierarchical travel network. Our results enable a comparison of the processes that drive the invasion of Omicron and other VOCs across multiple spatial scales.

Immunovirological and environmental screening reveals actionable risk factors for fatal COVID-19 during post-vaccination nursing home outbreaks.

Coronavirus Disease 2019 (COVID-19) vaccination has resulted in excellent protection against fatal disease, including in older adults. However, risk factors for post-vaccination fatal COVID-19 are largely unknown. We comprehensively studied three large nursing home outbreaks (20-35% fatal cases among residents) by combining severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) aerosol monitoring, whole-genome phylogenetic analysis and immunovirological profiling of nasal mucosa by digital nCounter transcriptomics. Phylogenetic investigations indicated that each outbreak stemmed from a single introduction event, although with different variants (Delta, Gamma and Mu). SARS-CoV-2 was detected in aerosol samples up to 52 d after the initial infection. Combining demographic, immune and viral parameters, the best predictive models for mortality comprised IFNB1 or age, viral ORF7a and ACE2 receptor transcripts. Comparison with published pre-vaccine fatal COVID-19 transcriptomic and genomic signatures uncovered a unique IRF3 low/IRF7 high immune signature in post-vaccine fatal COVID-19 outbreaks. A multi-layered strategy, including environmental sampling, immunomonitoring and early antiviral therapy, should be considered to prevent post-vaccination COVID-19 mortality in nursing homes.

Phylogeographic reconstruction of the emergence and spread of Powassan virus in the northeastern United States.

Powassan virus is an emerging tick-borne virus of concern for public health, but very little is known about its transmission patterns and ecology. Here, we expanded the genomic dataset by sequencing 279 Powassan viruses isolated from Ixodes scapularis ticks from the northeastern United States. Our phylogeographic reconstructions revealed that Powassan virus lineage II was likely introduced or emerged from a relict population in the Northeast between 1940 and 1975. Sequences strongly clustered by sampling location, suggesting a highly focal geographical distribution. Our analyses further indicated that Powassan virus lineage II emerged in the northeastern United States mostly following a south-to-north pattern, with a weighted lineage dispersal velocity of ~3 km/y. Since the emergence in the Northeast, we found an overall increase in the effective population size of Powassan virus lineage II, but with growth stagnating during recent years. The cascading effect of population expansion of white-tailed deer and I. scapularis populations likely facilitated the emergence of Powassan virus in the northeastern United States.

Variant-specific introduction and dispersal dynamics of SARS-CoV-2 in New York City - from Alpha to Omicron.

Since the latter part of 2020, SARS-CoV-2 evolution has been characterised by the emergence of viral variants associated with distinct biological characteristics. While the main research focus has centred on the ability of new variants to increase in frequency and impact the effective reproductive number of the virus, less attention has been placed on their relative ability to establish transmission chains and to spread through a geographic area. Here, we describe a phylogeographic approach to estimate and compare the introduction and dispersal dynamics of the main SARS-CoV-2 variants - Alpha, Iota, Delta, and Omicron - that circulated in the New York City area between 2020 and 2022. Notably, our results indicate that Delta had a lower ability to establish sustained transmission chains in the NYC area and that Omicron (BA.1) was the variant fastest to disseminate across the study area. The analytical approach presented here complements non-spatially-explicit analytical approaches that seek a better understanding of the epidemiological differences that exist among successive SARS-CoV-2 variants of concern.