Colonization of the Mediterranean basin by the vector biting midge species Culicoides imicola: an old story

Abstract

Understanding the demographic history and genetic make-up of colonizing species is critical for inferring population sources and colonization routes. This is of main interest for designing accurate control measures in areas newly colonized by vector species of economically important pathogens. The biting midge Culicoides imicola is a major vector of orbiviruses to livestock. Historically, the distribution of this species was limited to the Afrotropical region. Entomological surveys first revealed the presence of C. imicola in the south of the Mediterranean basin by the 1970s. Following recurrent reports of massive bluetongue outbreaks since the 1990s, the presence of the species was confirmed in northern areas. In this study, we addressed the chronology and processes of C. imicola colonization in the Mediterranean basin. We characterized the genetic structure of its populations across Mediterranean and African regions using both mitochondrial and nuclear markers, and combined phylogeographical analyses with population genetics and approximate Bayesian computation. We found a west/east genetic differentiation between populations, occurring both within Africa and within the Mediterranean basin. We demonstrated that three of these groups had experienced demographic expansions in the Pleistocene, probably because of climate changes during this period. Finally, we showed that C. imicola could have colonized the Mediterranean basin in the Late Pleistocene or Early Holocene through a single event of introduction; however, we cannot exclude the hypothesis involving two routes of colonization. Thus, the recent bluetongue outbreaks are not linked to C. imicola colonization event, but rather to biological changes in the vector or the virus.

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

“…Within Europe, it has been hypothesized that changes in the northern limits of C. imicola Kieffer in the Mediterranean basin have occurred and coincided with an unprecedented expansion of BTV in this region131415. This hypothesis is challenged by recent genetic analyses that supported a long-time presence of C. imicola in the Mediterranean basin1617. Culicoides imicola is the primary afrotropical vector species of BTV and African horse sickness virus (see review in1819).…”

First molecular identification of the vertebrate hosts of Culicoides imicola in Europe and a review of its blood‐feeding patterns worldwide: implications for the transmission of bluetongue disease and African horse sickness

“…Thus, the present results provide support for the feasibility of the COI marker as a barcoding region for use in the identification of C. imicola (Harrup et al ., ). Along with other genetic markers, study of the genetic diversity of the COI region of C. imicola has been used to examine the current distribution and colonization routes of this species in Europe (Jacquet et al ., , ). On the basis of sequences from 225 specimens collected in Europe and Africa, Jacquet et al .…”

DNA barcoding and surveillance sampling strategies for Culicoides biting midges (Diptera: Ceratopogonidae) in southern India

“…In addition, three publically available sequences (GenBank: AF080528, AF080529 and AF080536) labelled as C. imicola but with sequences differences of 2.9, 3.7 and 7.5 % respectively to the nearest other C. imicola sequence have been highlighted as likely to be the result of misidentification, cross-contamination or poor sequence quality. Genetic divergence and population structure within C. imicola , the principal Afrotropical vector of BTV, are subject to on-going investigations [80, 81] that will assist in clarifying the status of this pan-continental species.…”

“…This is particularly the case in India with numerous publications citing the presence of C. schultzei [12–14, 81–86], despite the fact that C. schultzei is an Afrotropical species while the type-locality of C. oxystoma is Kolkata in India. These two species are, however, both morphologically [18, 87] and genetically [9, 76, 88] distinct, and current evidence agrees with the earlier proposal by Cornet [89] that C. oxystoma is the species present in India.…”