Geographic distribution of the V1016G knockdown resistance mutation in Aedes albopictus: a warning bell for Europe

Abstract

Background Colonization of large part of Europe by the Asian tiger mosquito Aedes albopictus is causing autochthonous transmission of chikungunya and dengue exotic arboviruses. While pyrethroids are recommended only to reduce/limit transmission, they are widely implemented to reduce biting nuisance and to control agricultural pests, increasing the risk of insurgence of resistance mechanisms. Worryingly, pyrethroid resistance (with mortality < 70%) was recently reported in Ae. albopictus populations from Italy and Spain and associated with the V1016G point mutation in the voltage-sensitive sodium channel gene conferring knockdown resistance (kdr). Genotyping pyrethroid resistance-associated kdr mutations in field mosquito samples represents a powerful approach to detect early signs of resistance without the need for carrying out phenotypic bioassays which require availability of live mosquitoes, dedicated facilities and appropriate expertise. Methods Here we report results on the PCR-genotyping of the V1016G mutation in 2530 Ae. albopictus specimens from 69 sampling sites in 19 European countries. Results The mutation was identified in 12 sites from nine countries (with allele frequencies ranging from 1 to 8%), mostly distributed in two geographical clusters. The western cluster includes Mediterranean coastal sites from Italy, France and Malta as well as single sites from both Spain and Switzerland. The eastern cluster includes sites on both sides of the Black Sea in Bulgaria, Turkey and Georgia as well as one site from Romania. These results are consistent with genomic data showing high connectivity and close genetic relationship among West European populations and a major barrier to gene flow between West European and Balkan populations. Conclusions The results of this first effort to map kdr mutations in Ae. albopictus on a continental scale show a widespread presence of the V1016G allele in Europe, although at lower frequencies than those previously reported from Italy. This represents a wake-up call for mosquito surveillance programs in Europe to include PCR-genotyping of pyrethroid resistance alleles, as well as phenotypic resistance assessments, in their routine activities. Graphical Abstract

Diversity and distribution of sodium channel mutations in Aedes albopictus (Diptera: Culicidae)

“…albopictus , the literature in 2022 and 2023 mostly focuses on survey data. The geographic distribution of the V1016G mutation was mapped across Europe by Pichler et al (2022) who found it in 8 countries where it had not been found before. Twelve studies assessed associations between non-synonymous mutations and resistance levels identified in bioassays by comparing genotypes of dead and surviving mosquitoes ( Table 5 ).…”

“…Similar studies could be conducted on the V1016G mutation which has also been shown to confer high levels of pyrethroid resistance in Ae . albopictus ( Kasai et al 2019 , Pichler et al 2019 ) and is becoming highly prevalent throughout multiple locations in Europe ( Pichler et al 2022 ).…”

Molecular monitoring of insecticide resistance in major disease vectors in Armenia

“…Aedes albopictus mosquitoes were tested for a total of six kdr mutations linked to pyrethroid resistance (V1010G, V1010GI, I1532T, F1534C, F1534L, F1534S), and the V1016G mutation was detected, albeit at a very low frequency (1.9%; 1 heterozygote mosquito). Although no previous data are available in Armenia, the presence of V1016G mutation has been previously recorded in neighbouring countries, at a frequency of 1.0% in Georgia and 1.9% in Turkey, and this is concerning for neighbouring countries like Iran [ 44 ], where this vector is present, but also for Europe in general [ 45 ]. The occurrence of V1016G, despite its low frequency, is alarming regarding future further resistance spread.…”

High frequency of Voltage-gated sodium channel (VGSC) gene mutations in Aedes albopictus (Diptera: Culicidae) suggest rapid insecticide resistance evolution in Shanghai, China

“…The VGSC gene of Ae . albopictus contains four domains (I–IV), and nonsynonymous point mutations have been found only in Domain II, III, and IV [ 17 , 32 ]. To detect point mutations in VGSC , fragments from Domain II, III, and IV were amplified via PCR under the same conditions.…”