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

Type Article
Date 2021-12
Language English
Author(s) Mignotte Antoine1, 2, Garros Claire1, 2, Dellicour Simon3, 4, Jacquot MaudeORCID3, 5, Gilbert Marius3, Gardès Laetitia1, 6, Balenghien Thomas1, 7, 8, Duhayon Maxime1, 2, Rakotoarivony Ignace1, 2, de Wavrechin Maïa1, 2, Huber Karine1
Affiliation(s) 1 : ASTRE, Univ Montpellier, Cirad, INRAE, Montpellier, France
2 : Cirad, UMR ASTRE, 34398, Montpellier, France
3 : Spatial Epidemiology Lab (SpELL), Université Libre de Bruxelles, CP160/12, 50, av. FD Roosevelt, 1050, Bruxelles, Belgium
4 : Department of Microbiology, Immunology and Transplantation, Rega Institute, KU Leuven, Herestraat 49, 3000, Leuven, Belgium
5 : UMR EPIA, Université Clermont Auvergne, INRAE, VetAgro Sup, 63122, Saint-Genès-Champanelle, France
6 : Cirad, UMR ASTRE, 97170, Petit-Bourg, Guadeloupe, France
7 : Cirad, UMR ASTRE, 10100, Rabat, Morocco
8 : Unité Microbiologie, immunologie et maladies contagieuses, Institut Agronomique et Vétérinaire Hassan II, 10100, Rabat-Instituts, Morocco
Source Parasites & Vectors (1756-3305) (Springer Science and Business Media LLC), 2021-12 , Vol. 14 , N. 1 , P. 93 (14p.)
DOI 10.1186/s13071-020-04522-3
Keyword(s) Culicoides obsoletus, Landscape genetics, Microsatellite, Dispersal, Palearctic region
Abstract

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.

Full Text
File Pages Size Access
Publisher's official version 14 2 MB Open access
Table S1. Sampling sites and associated genetic diversity. n Sample size, Ho observed heterozygosity, Hs expected heterozygosity, FIS fixation index. 11 KB Open access
Table S2. Reference sequences used for specific assignation. 9 KB Open access
Table S3. Origin and numbers of individuals used to build up the DNA library necessary for the development of the microsatellite markers. 8 KB Open access
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. 14 KB Open access
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). 1 MB Open access
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. ... 65 KB Open access
Figure S3. Analytical workflow. 137 KB Open access
Table S5. Genetic diversity by locus. Ho Observed heterozygosity, Hs expected heterozygosity, FIS fixation index, SAD short alleles dominance. 9 KB Open access
Figure S4. Isolation by distance analyses: density plots, Mantel tests and linear regressions performed with each inter-individual genetic distance considered in this study. 250 KB Open access
Figure S5. Identification of the optimal number of genetic clusters (K) inferred by STRUCTURE using the δ(K) and L’(K) methods. 61 KB Open access
Figure S6. Population genetic structure results by clustering analyses performed STRUCTURE. A specific color has been assigned to each inferred genetic cluster. 5 MB Open access
Table S6. Results of univariate analyses: determination coefficients (R2) estimated from univariate regressions between genetic and environmental distances. [C] indicates that the considered environ 9 KB Open access
Top of the page

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.). Publisher's official version : https://doi.org/10.1186/s13071-020-04522-3 , Open Access version : https://archimer.ifremer.fr/doc/00678/79022/