Publications by authors named "Maude Jacquot"

9 Publications

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High dispersal capacity of Culicoides obsoletus (Diptera: Ceratopogonidae), vector of bluetongue and Schmallenberg viruses, revealed by landscape genetic analyses.

Parasit Vectors 2021 Feb 3;14(1):93. Epub 2021 Feb 3.

ASTRE, Univ Montpellier, Cirad, INRAE, Montpellier, France.

Background: In the last two decades, recurrent epizootics of bluetongue virus and Schmallenberg virus have been reported in the western Palearctic region. These viruses affect domestic cattle, sheep, goats and wild ruminants and are transmitted by native hematophagous midges of the genus Culicoides (Diptera: Ceratopogonidae). Culicoides dispersal is known to be stratified, i.e. due to a combination of dispersal processes occurring actively at short distances and passively or semi-actively at long distances, allowing individuals to jump hundreds of kilometers.

Methods: Here, we aim to identify the environmental factors that promote or limit gene flow of Culicoides obsoletus, an abundant and widespread vector species in Europe, using an innovative framework integrating spatial, population genetics and statistical approaches. A total of 348 individuals were sampled in 46 sites in France and were genotyped using 13 newly designed microsatellite markers.

Results: We found low genetic differentiation and a weak population structure for C. obsoletus across the country. Using three complementary inter-individual genetic distances, we did not detect any significant isolation by distance, but did detect significant anisotropic isolation by distance on a north-south axis. We employed a multiple regression on distance matrices approach to investigate the correlation between genetic and environmental distances. Among all the environmental factors that were tested, only cattle density seems to have an impact on C. obsoletus gene flow.

Conclusions: The high dispersal capacity of C. obsoletus over land found in the present study calls for a re-evaluation of the impact of Culicoides on virus dispersal, and highlights the urgent need to better integrate molecular, spatial and statistical information to guide vector-borne disease control.
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http://dx.doi.org/10.1186/s13071-020-04522-3DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7860033PMC
February 2021

"Frozen evolution" of an RNA virus suggests accidental release as a potential cause of arbovirus re-emergence.

PLoS Biol 2020 04 28;18(4):e3000673. Epub 2020 Apr 28.

MRC-University of Glasgow Centre for Virus Research, Glasgow, United Kingdom.

The mechanisms underlying virus emergence are rarely well understood, making the appearance of outbreaks largely unpredictable. Bluetongue virus serotype 8 (BTV-8), an arthropod-borne virus of ruminants, emerged in livestock in northern Europe in 2006, spreading to most European countries by 2009 and causing losses of billions of euros. Although the outbreak was successfully controlled through vaccination by early 2010, puzzlingly, a closely related BTV-8 strain re-emerged in France in 2015, triggering a second outbreak that is still ongoing. The origin of this virus and the mechanisms underlying its re-emergence are unknown. Here, we performed phylogenetic analyses of 164 whole BTV-8 genomes sampled throughout the two outbreaks. We demonstrate consistent clock-like virus evolution during both epizootics but found negligible evolutionary change between them. We estimate that the ancestor of the second outbreak dates from the height of the first outbreak in 2008. This implies that the virus had not been replicating for multiple years prior to its re-emergence in 2015. Given the absence of any known natural mechanism that could explain BTV-8 persistence over this long period without replication, we hypothesise that the second outbreak could have been initiated by accidental exposure of livestock to frozen material contaminated with virus from approximately 2008. Our work highlights new targets for pathogen surveillance programmes in livestock and illustrates the power of genomic epidemiology to identify pathways of infectious disease emergence.
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http://dx.doi.org/10.1371/journal.pbio.3000673DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7188197PMC
April 2020

Contrasting selective patterns across the segmented genome of bluetongue virus in a global reassortment hotspot.

Virus Evol 2019 Jul 5;5(2):vez027. Epub 2019 Aug 5.

Institute of Biodiversity, Animal Health and Comparative Medicine, Boyd Orr Centre for Population and Ecosystem Health, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow, UK.

For segmented viruses, rapid genomic and phenotypic changes can occur through the process of reassortment, whereby co-infecting strains exchange entire segments creating novel progeny virus genotypes. However, for many viruses with segmented genomes, this process and its effect on transmission dynamics remain poorly understood. Here, we assessed the consequences of reassortment for selection on viral diversity through time using bluetongue virus (BTV), a segmented arbovirus that is the causative agent of a major disease of ruminants. We analysed ninety-two BTV genomes isolated across four decades from India, where BTV diversity, and thus opportunities for reassortment, are among the highest in the world. Our results point to frequent reassortment and segment turnover, some of which appear to be driven by selective sweeps and serial hitchhiking. Particularly, we found evidence for a recent selective sweep affecting segment 5 and its encoded NS1 protein that has allowed a single variant to essentially invade the full range of BTV genomic backgrounds and serotypes currently circulating in India. In contrast, diversifying selection was found to play an important role in maintaining genetic diversity in genes encoding outer surface proteins involved in virus interactions (VP2 and VP5, encoded by segments 2 and 6, respectively). Our results support the role of reassortment in driving rapid phenotypic change in segmented viruses and generate testable hypotheses for experiments aiming at understanding the specific mechanisms underlying differences in fitness and selection across viral genomes.
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http://dx.doi.org/10.1093/ve/vez027DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6680063PMC
July 2019

Endemic infection can shape exposure to novel pathogens: Pathogen co-occurrence networks in the Serengeti lions.

Ecol Lett 2019 Jun 12;22(6):904-913. Epub 2019 Mar 12.

Department of Veterinary Population Medicine, University of Minnesota, 1365 Gortner Avenue, St Paul, MN, 55108, USA.

Pathogens are embedded in a complex network of microparasites that can collectively or individually alter disease dynamics and outcomes. Endemic pathogens that infect an individual in the first years of life, for example, can either facilitate or compete with subsequent pathogens thereby exacerbating or ameliorating morbidity and mortality. Pathogen associations are ubiquitous but poorly understood, particularly in wild populations. We report here on 10 years of serological and molecular data in African lions, leveraging comprehensive demographic and behavioural data to test if endemic pathogens shape subsequent infection by epidemic pathogens. We combine network and community ecology approaches to assess broad network structure and characterise associations between pathogens across spatial and temporal scales. We found significant non-random structure in the lion-pathogen co-occurrence network and identified both positive and negative associations between endemic and epidemic pathogens. Our results provide novel insights on the complex associations underlying pathogen co-occurrence networks.
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http://dx.doi.org/10.1111/ele.13250DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7163671PMC
June 2019

Bluetongue virus spread in Europe is a consequence of climatic, landscape and vertebrate host factors as revealed by phylogeographic inference.

Proc Biol Sci 2017 Oct;284(1864)

College of Medical, Veterinary and Life Sciences, Institute of Biodiversity, Animal Health and Comparative Medicine, Boyd Orr Centre for Population and Ecosystem Health, University of Glasgow, Glasgow, UK

Spatio-temporal patterns of the spread of infectious diseases are commonly driven by environmental and ecological factors. This is particularly true for vector-borne diseases because vector populations can be strongly affected by host distribution as well as by climatic and landscape variables. Here, we aim to identify environmental drivers for bluetongue virus (BTV), the causative agent of a major vector-borne disease of ruminants that has emerged multiple times in Europe in recent decades. In order to determine the importance of climatic, landscape and host-related factors affecting BTV diffusion across Europe, we fitted different phylogeographic models to a dataset of 113 time-stamped and geo-referenced BTV genomes, representing multiple strains and serotypes. Diffusion models using continuous space revealed that terrestrial habitat below 300 m altitude, wind direction and higher livestock densities were associated with faster BTV movement. Results of discrete phylogeographic analysis involving generalized linear models broadly supported these findings, but varied considerably with the level of spatial partitioning. Contrary to common perception, we found no evidence for average temperature having a positive effect on BTV diffusion, though both methodological and biological reasons could be responsible for this result. Our study provides important insights into the drivers of BTV transmission at the landscape scale that could inform predictive models of viral spread and have implications for designing control strategies.
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http://dx.doi.org/10.1098/rspb.2017.0919DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5647287PMC
October 2017

Linking social and spatial networks to viral community phylogenetics reveals subtype-specific transmission dynamics in African lions.

J Anim Ecol 2017 10 10;86(6):1469-1482. Epub 2017 Oct 10.

Department of Veterinary Population Medicine, University of Minnesota, St Paul, MN, USA.

Heterogeneity within pathogen species can have important consequences for how pathogens transmit across landscapes; however, discerning different transmission routes is challenging. Here, we apply both phylodynamic and phylogenetic community ecology techniques to examine the consequences of pathogen heterogeneity on transmission by assessing subtype-specific transmission pathways in a social carnivore. We use comprehensive social and spatial network data to examine transmission pathways for three subtypes of feline immunodeficiency virus (FIV ) in African lions (Panthera leo) at multiple scales in the Serengeti National Park, Tanzania. We used FIV molecular data to examine the role of social organization and lion density in shaping transmission pathways and tested to what extent vertical (i.e., father- and/or mother-offspring relationships) or horizontal (between unrelated individuals) transmission underpinned these patterns for each subtype. Using the same data, we constructed subtype-specific FIV co-occurrence networks and assessed what combination of social networks, spatial networks or co-infection best structured the FIV network. While social organization (i.e., pride) was an important component of FIV transmission pathways at all scales, we find that FIV subtypes exhibited different transmission pathways at within- and between-pride scales. A combination of social and spatial networks, coupled with consideration of subtype co-infection, was likely to be important for FIV transmission for the two major subtypes, but the relative contribution of each factor was strongly subtype-specific. Our study provides evidence that pathogen heterogeneity is important in understanding pathogen transmission, which could have consequences for how endemic pathogens are managed. Furthermore, we demonstrate that community phylogenetic ecology coupled with phylodynamic techniques can reveal insights into the differential evolutionary pressures acting on virus subtypes, which can manifest into landscape-level effects.
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http://dx.doi.org/10.1111/1365-2656.12751DOI Listing
October 2017

Multiple independent transmission cycles of a tick-borne pathogen within a local host community.

Sci Rep 2016 08 8;6:31273. Epub 2016 Aug 8.

INRA, UR346 Epidémiologie animale, Saint Genès Champanelle, France.

Many pathogens are maintained by multiple host species and involve multiple strains with potentially different phenotypic characteristics. Disentangling transmission patterns in such systems is often challenging, yet investigating how different host species contribute to transmission is crucial to properly assess and manage disease risk. We aim to reveal transmission cycles of bacteria within the Borrelia burgdorferi species complex, which include Lyme disease agents. We characterized Borrelia genotypes found in 488 infected Ixodes ricinus nymphs collected in the Sénart Forest located near Paris (France). These genotypes were compared to those observed in three sympatric species of small mammals and network analyses reveal four independent transmission cycles. Statistical modelling shows that two cycles involving chipmunks, an introduced species, and non-sampled host species such as birds, are responsible for the majority of tick infections. In contrast, the cycle involving native bank voles only accounts for a small proportion of infected ticks. Genotypes associated with the two primary transmission cycles were isolated from Lyme disease patients, confirming the epidemiological threat posed by these strains. Our work demonstrates that combining high-throughput sequence typing with networks tools and statistical modeling is a promising approach for characterizing transmission cycles of multi-host pathogens in complex ecological settings.
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http://dx.doi.org/10.1038/srep31273DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4976386PMC
August 2016

Comparative population genomics of the Borrelia burgdorferi species complex reveals high degree of genetic isolation among species and underscores benefits and constraints to studying intra-specific epidemiological processes.

PLoS One 2014 10;9(4):e94384. Epub 2014 Apr 10.

INRA, UR346 Epidémiologie Animale, Saint Genès Champanelle, France.

Lyme borreliosis, one of the most frequently contracted zoonotic diseases in the Northern Hemisphere, is caused by bacteria belonging to different genetic groups within the Borrelia burgdorferi species complex, which are transmitted by ticks among various wildlife reservoirs, such as small mammals and birds. These features make the Borrelia burgdorferi species complex an attractive biological model that can be used to study the diversification and the epidemiology of endemic bacterial pathogens. We investigated the potential of population genomic approaches to study these processes. Sixty-three strains belonging to three species within the Borrelia burgdorferi complex were isolated from questing ticks in Alsace (France), a region where Lyme disease is highly endemic. We first aimed to characterize the degree of genetic isolation among the species sampled. Phylogenetic and coalescent-based analyses revealed clear delineations: there was a ∼50 fold difference between intra-specific and inter-specific recombination rates. We then investigated whether the population genomic data contained information of epidemiological relevance. In phylogenies inferred using most of the genome, conspecific strains did not cluster in clades. These results raise questions about the relevance of different strategies when investigating pathogen epidemiology. For instance, here, both classical analytic approaches and phylodynamic simulations suggested that population sizes and migration rates were higher in B. garinii populations, which are normally associated with birds, than in B. burgdorferi s.s. populations. The phylogenetic analyses of the infection-related ospC gene and its flanking region provided additional support for this finding. Traces of recombination among the B. burgdorferi s.s. lineages and lineages associated with small mammals were found, suggesting that they shared the same hosts. Altogether, these results provide baseline evidence that can be used to formulate hypotheses regarding the host range of B. burgdorferi lineages based on population genomic data.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0094384PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3993988PMC
December 2014

High-throughput sequence typing reveals genetic differentiation and host specialization among populations of the Borrelia burgdorferi species complex that infect rodents.

PLoS One 2014 12;9(2):e88581. Epub 2014 Feb 12.

INRA, UR346 Épidémiologie Animale, Saint Genès Champanelle, France.

Lyme disease is a zoonosis caused by various species belonging to the Borrelia burgdorferi bacterial species complex. These pathogens are transmitted by ticks and infect multiple, taxonomically distinct, host species. From an epidemiological perspective, it is important to determine whether genetic variants within the species complex are able to spread freely through the whole host community or, instead, if certain variants are restricted to particular hosts. To this end, we characterized the genotypes of members of the B. burgdorferi species complex; the bacteria were isolated from more than two hundred individuals captured in the wild and belonging to three different rodent host species. For each individual, we used a high-throughput approach to amplify and sequence rplB, a housekeeping gene, and ospC, which is involved in infection. This approach allowed us to evaluate the genetic diversity both within and among species in the B. burgdorferi species complex. Strong evidence of genetic differentiation among host species was revealed by both genes, even though they are, a priori, not constrained by the same selective pressures. These data are discussed in the context of the advancements made possible by multi-locus high-throughput sequencing and current knowledge of Lyme disease epidemiology.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0088581PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3922933PMC
January 2015