Provenance and competence for CHIKV and DENV of Aedes albopictus populations

Aedes albopictus is one of the world’s most hazardous invasive species, increasingly implicated in the autochthonous transmission of Chikungunya (CHIKV) and Dengue (DENV) viruses in newly colonized areas. Since invading the Mediterranean Basin several in the early 1980s, recurrent introductions of distinct lineages have driven extensive genomic admixture within adventive populations. This study investigates whether and how the complex dynamics of these diverse genetic backgrounds have shaped variations in vector competence for CHIKV, DENV, and Zika (ZIKV) viruses. Using highly polymorphic simple sequence repeat (SSR) markers, we genotyped Ae. Albopictus samples from an ancestral population (Guangzhou, China) and ten adventive populations across five Mediterranean regions (Southern Switzerland, Northern/Central Italy, the Balkans, and Greece). Genetic ancestry and demographic histories were inferred using Bayesian STRUCTURE (v2.3.2.0) and DIYABC-RF. The association between population ancestry and vector competence for CHIKV (06.21), DENV-1, and ZIKV (PE243) was assessed using infection rate, dissemination efficiency, and transmission efficiency indices, analyzed via univariate and multivariate models. Combining historical records with demographic models revealed that the establishment of Ae. Albopictus in the Mediterranean was driven by chaotic, discontinuous lineage introductions and admixture events, resulting in high spatial and ancestry heterogeneity. Notably, this genetic heterogeneity significantly influences vector competence, in particular for CHIKV and DENV. Interestingly, populations in neighboring geographical areas with distinct ancestries exhibited drastically different competence profiles, whereas geographically distant populations sharing genetic ancestry displayed similar vector competence for CHIKV and DENV. Our findings demonstrate that the complex population dynamics and colonization history of Ae. Albopictus contributes to variation in vector competence, altering the geographical landscape of arboviral risk. These results underscore the urgent need for localized, geographically tailored vector control strategies in Europe, a region facing a rising trend of both imported and autochthonous arboviral infections.