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Range expansion of the Bluetongue vector, Culicoides imicola, in continental France likely due to rare wind-transport events.

ABSTRACT: The role of the northward expansion of Culicoides imicola Kieffer in recent and unprecedented outbreaks of Culicoides-borne arboviruses in southern Europe has been a significant point of contention. We combined entomological surveys, movement simulations of air-borne particles, and population genetics to reconstruct the chain of events that led to a newly colonized French area nestled at the northern foot of the Pyrenees. Simulating the movement of air-borne particles evidenced frequent wind-transport events allowing, within at most 36?hours, the immigration of midges from north-eastern Spain and Balearic Islands, and, as rare events, their immigration from Corsica. Completing the puzzle, population genetic analyses discriminated Corsica as the origin of the new population and identified two successive colonization events within west-Mediterranean basin. Our findings are of considerable importance when trying to understand the invasion of new territories by expanding species.

SUBMITTER: Jacquet S

PROVIDER: S-EPMC4893744 | biostudies-literature | 2016 Jun

REPOSITORIES: biostudies-literature

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Range expansion of the Bluetongue vector, Culicoides imicola, in continental France likely due to rare wind-transport events.

Jacquet Stéphanie S Huber Karine K Pagès Nonito N Talavera Sandra S Burgin Laura E LE Carpenter Simon S Sanders Christopher C Dicko Ahmadou H AH Djerbal Mouloud M Goffredo Maria M Lhor Youssef Y Lucientes Javier J Miranda-Chueca Miguel A MA Pereira Da Fonseca Isabel I Ramilo David W DW Setier-Rio Marie-Laure ML Bouyer Jérémy J Chevillon Christine C Balenghien Thomas T Guis Hélène H Garros Claire C

Scientific reports 20160606

The role of the northward expansion of Culicoides imicola Kieffer in recent and unprecedented outbreaks of Culicoides-borne arboviruses in southern Europe has been a significant point of contention. We combined entomological surveys, movement simulations of air-borne particles, and population genetics to reconstruct the chain of events that led to a newly colonized French area nestled at the northern foot of the Pyrenees. Simulating the movement of air-borne particles evidenced frequent wind-tra ...[more]

PMID: 27263862

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Project description:Bluetongue virus (BTV) and epizootic haemorrhagic disease virus (EHDV) are related orbiviruses, transmitted between their ruminant hosts primarily by certain haematophagous midge vectors (Culicoides spp.). The larger of the BTV outer-capsid proteins, 'VP2', can be cleaved by proteases (including trypsin or chymotrypsin), forming infectious subviral particles (ISVP) which have enhanced infectivity for adult Culicoides, or KC cells (a cell-line derived from C. sonorensis). We demonstrate that VP2 present on purified virus particles from 3 different BTV strains can also be cleaved by treatment with saliva from adult Culicoides. The saliva proteins from C. sonorensis (a competent BTV vector), cleaved BTV-VP2 more efficiently than those from C. nubeculosus (a less competent/non-vector species). Electrophoresis and mass spectrometry identified a trypsin-like protease in C. sonorensis saliva, which was significantly reduced or absent from C. nubeculosus saliva. Incubating purified BTV-1 with C. sonorensis saliva proteins also increased their infectivity for KC cells ∼10 fold, while infectivity for BHK cells was reduced by 2-6 fold. Treatment of an 'eastern' strain of EHDV-2 with saliva proteins of either C. sonorensis or C. nubeculosus cleaved VP2, but a 'western' strain of EHDV-2 remained unmodified. These results indicate that temperature, strain of virus and protein composition of Culicoides saliva (particularly its protease content which is dependent upon vector species), can all play a significant role in the efficiency of VP2 cleavage, influencing virus infectivity. Saliva of several other arthropod species has previously been shown to increase transmission, infectivity and virulence of certain arboviruses, by modulating and/or suppressing the mammalian immune response. The findings presented here, however, demonstrate a novel mechanism by which proteases in Culicoides saliva can also directly modify the orbivirus particle structure, leading to increased infectivity specifically for Culicoides cells and, in turn, efficiency of transmission to the insect vector.

Project description:The possibility that outbreaks of bluetongue (BT) and African horse sickness (AHS) might occur via long-distance wind dispersion (LDWD) of their insect vector (Culicoides spp.) was proposed by R. F. Sellers in a series of papers published between 1977 and 1991. These investigated the role of LDWD by means of visual examination of the wind direction of synoptic weather charts. Based on the hypothesis that simple wind direction analysis, which does not allow for wind speed, might have led to spurious conclusions, we reanalyzed six of the outbreak scenarios described in Sellers' papers. For this reanalysis, we used a custom-built Big Data application ("TAPPAS") which couples a user-friendly web-interface with an established atmospheric dispersal model ("HYSPLIT"), thus enabling more sophisticated modeling than was possible when Sellers undertook his analyzes. For the two AHS outbreaks, there was strong support from our reanalysis of the role of LDWD for that in Spain (1966), and to a lesser degree, for the outbreak in Cyprus (1960). However, for the BT outbreaks, the reassessments were more complex, and for one of these (western Turkey, 1977) we could discount LDWD as the means of direct introduction of the virus. By contrast, while the outbreak in Cyprus (1977) showed LDWD was a possible means of introduction, there is an apparent inconsistency in that the outbreaks were localized while the dispersion events covered much of the island. For Portugal (1956), LDWD from Morocco on the dates suggested by Sellers is very unlikely to have been the pathway for introduction, and for the detection of serotype 2 in Florida (1982), LDWD from Cuba would require an assumption of a lengthy survival time of the midges in the air column. Except for western Turkey, the BT reanalyses show the limitation of LDWD modeling when used by itself, and indicates the need to integrate susceptible host population distribution (and other covariate) data into the modeling process. A further refinement, which will become increasingly important to assess LDWD, will be the use of virus and vector genome sequence data collected from potential source and the incursion sites.

Project description:BackgroundThe spread of Bluetongue virus (BTV) among ruminants is caused by movement of infected host animals or by movement of infected Culicoides midges, the vector of BTV. Biologically plausible models of Culicoides dispersal are necessary for predicting the spread of BTV and are important for planning control and eradication strategies.MethodsA spatially-explicit simulation model which captures the two underlying population mechanisms, population dynamics and movement, was developed using extensive data from a trapping program for C. brevitarsis on the east coast of Australia. A realistic midge flight sub-model was developed and the annual incursion and population establishment of C. brevitarsis was simulated. Data from the literature was used to parameterise the model.ResultsThe model was shown to reproduce the spread of C. brevitarsis southwards along the east Australian coastline in spring, from an endemic population to the north. Such incursions were shown to be reliant on wind-dispersal; Culicoides midge active flight on its own was not capable of achieving known rates of southern spread, nor was re-emergence of southern populations due to overwintering larvae. Data from midge trapping programmes were used to qualitatively validate the resulting simulation model.ConclusionsThe model described in this paper is intended to form the vector component of an extended model that will also include BTV transmission. A model of midge movement and population dynamics has been developed in sufficient detail such that the extended model may be used to evaluate the timing and extent of BTV outbreaks. This extended model could then be used as a platform for addressing the effectiveness of spatially targeted vaccination strategies or animal movement bans as BTV spread mitigation measures, or the impact of climate change on the risk and extent of outbreaks. These questions involving incursive Culicoides spread cannot be simply addressed with non-spatial models.

Project description:BackgroundBluetongue disease, caused by bluetongue virus serotype 8 (BTV-8), appeared for the first time in the northern part of Europe in 2006, and subsequently rapidly spread causing severe economic losses to the farming industry. The implicated vectors of BTV in Europe are Culicoides species within the subgenus Avaritia (C. chiopterus, C. dewulfi, C. obsoletus and C. scoticus). Epidemiological data from Switzerland have shown that BTV, whose spread was eliminated at an early stage by vaccination campaigns, had not been circulating among livestock at higher altitudes where other species dominate the Culicoides fauna. In this study, we investigated the extent that Culicoides spp. prevailing at higher altitudes (mainly C. grisescens) can act as vectors for BTV.MethodsCulicoides were collected at farms in the pre-alpine region (two sites at 1550 m above sea level, masl, referred to as pre-alpine I; one site at 2030 masl, pre-alpine II) and, for comparative purposes, from the Swiss Plateau (one site, 650 masl). They were fed on bovine blood/BTV suspensions (BTV-1, 4 or 8) and incubated for eight days under a fluctuating temperature regime (13-25 °C, mean 19 °C), reflecting a mid-summer warm spell in the pre-alpine region. Susceptibility to BTV transmission was assessed from head homogenates by RT-qPCR and virus isolation.ResultsOverall, 9196 female Culicoides were exposed to the three BTV strains through an artificial membrane, with feeding rates of 14-27%. Survival rates of blood-engorged Culicoides females at eight days post-infection depended on both virus serotype and altitude of origin. Virus dissemination (Cq ≤ the cut-off value as determined by serial virus dilutions) was confirmed only for BTV-1 in C. scoticus (dissemination efficiency 22.5%; 9/40) and C. obsoletus (5.6%; 1/18) from the Swiss Plateau area. There was no strong evidence of susceptibility to infection for Culicoides from the pre-alpine area when fed with all BTV strains (BTV-1, 4 and 8).ConclusionsThis study confirms the susceptibility of C. scoticus and C. obsoletus to BTV-1 infection, including under cooler temperatures. Culicoides grisescens, which is highly abundant at higher altitudes, cannot be considered a potential vector under these temperature conditions.

Dataset Information

Range expansion of the Bluetongue vector, Culicoides imicola, in continental France likely due to rare wind-transport events.

Publications

Range expansion of the Bluetongue vector, Culicoides imicola, in continental France likely due to rare wind-transport events.

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