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

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.

Keywords: Culicoides obsoletus; Dispersal; Landscape genetics; Microsatellite; Palearctic region.

Fig. 1a–d

Genetic clustering and genetic differentiation of Culicoides obsoletus. Results of the genetic clustering analyses performed with GENELAND (a) and STRUCTURE (b), as well as smoothing of pairwise measures performed with mapping averaged pairwise information (MAPI) and based on (c) Rousset’s (a_R) and (d) factorial correspondence analysis (FCA) inter-individual genetic distances. A specific color has been assigned to each genetic cluster in a and b. c, d Genetic dissimilarity is represented by a color scale ranging from red (lower genetic dissimilarity) to blue (higher genetic dissimilarity). The black circles indicate the sampling sites

Fig. 2a–c

Results of anisotropic isolation by distance analyses. Polar plots show the correlation between geographical projected distances by angle and inter-individual genetic distances [a_R (a), Loiselle’s kinship coefficient (LKC) (b), and FCA (c)]. The set of angles between 0 and 360 were then tested as angles that maximize isolation by distance. The projected distance matrix was calculated for each angle between all sampling sites, using the formula in the Methods. A linear regression of the genetic distances on the projected geographical distances obtained for each angle was then performed. The angle that maximizes the R² of this regression with a positive regression coefficient was considered as the angle maximizing the isolation by distance signal

Fig. 3

Bearing analysis: correlation between genetic [a_R (a), LKC (b), and FCA (c)] and geographical distances as a function of the angle between sampling sites. Circles indicate significant values, crosses indicate non-significant values. E East, W west, S south, N north; for other abbreviations, see Figs. 1 and 2