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

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.

Keyword(s)

Culicoides obsoletus, Landscape genetics, Microsatellite, Dispersal, Palearctic region

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Table S1. Sampling sites and associated genetic diversity. n Sample size, Ho observed heterozygosity, Hs expected heterozygosity, FIS fixation index.
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Table S2. Reference sequences used for specific assignation.
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Table S3. Origin and numbers of individuals used to build up the DNA library necessary for the development of the microsatellite markers.
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Table S4. Primers of the 13 microsatellite markers used to genotype C. obsoletus populations. DYE Fluorochrome, TFm half denaturation temperature in degrees, bp base pairs.
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Figure S1. Environmental variables tested as potential factors that could impact inter-individual genetic differentiation of C. obsoletus in France (raster cell resolution: 0.04 arcmin).
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Figure S2. Map of wind direction averaged from 2000 to 2010. Sampling sites are represented by black points. The color scale represents the wind direction from 0 to 360 ° from north. ...
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Figure S3. Analytical workflow.
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Table S5. Genetic diversity by locus. Ho Observed heterozygosity, Hs expected heterozygosity, FIS fixation index, SAD short alleles dominance.
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Figure S4. Isolation by distance analyses: density plots, Mantel tests and linear regressions performed with each inter-individual genetic distance considered in this study.
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Figure S5. Identification of the optimal number of genetic clusters (K) inferred by STRUCTURE using the δ(K) and L’(K) methods.
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Figure S6. Population genetic structure results by clustering analyses performed STRUCTURE. A specific color has been assigned to each inferred genetic cluster.
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Table S6. Results of univariate analyses: determination coefficients (R2) estimated from univariate regressions between genetic and environmental distances. [C] indicates that the considered environ
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How to cite
Mignotte Antoine, Garros Claire, Dellicour Simon, Jacquot Maude, Gilbert Marius, Gardès Laetitia, Balenghien Thomas, Duhayon Maxime, Rakotoarivony Ignace, de Wavrechin Maïa, Huber Karine (2021). High dispersal capacity of Culicoides obsoletus (Diptera: Ceratopogonidae), vector of bluetongue and Schmallenberg viruses, revealed by landscape genetic analyses. Parasites & Vectors. 14 (1). 93 (14p.). https://doi.org/10.1186/s13071-020-04522-3, https://archimer.ifremer.fr/doc/00678/79022/

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