Vector competence of Aedes albopictus populations for chikungunya virus is shaped by their demographic history

Abstract

The mosquito Aedes albopictus is one of the most dangerous invasive species. Its worldwide spread has created health concerns as it is a major vector of arboviruses of public health significance such as chikungunya (CHIKV). Dynamics of different genetic backgrounds and admixture events may have impacted competence for CHIKV in adventive populations. Using microsatellites, we infer the genetic structure of populations across the expansion areas that we then associate with their competence for different CHIKV genotypes. Here we show that the demographic history of Ae. albopictus populations is a consequence of rapid complex patterns of historical lineage diversification and divergence that influenced their competence for CHIKV. The history of adventive populations is associated with CHIKV genotypes in a genotype-by-genotype interaction that impacts their vector competence. Thus, knowledge of the demographic history and vector competence of invasive mosquitoes is pivotal for assessing the risk of arbovirus outbreaks in newly colonized areas.

Fig. 1. Matrix of pairwise F_ST values among 25 Ae. albopictus population samples.

F_ST values highlighted with a white circle are not significantly different from zero (P > 0.05) after Bonferroni correction.

Fig. 2. Representation of the co-ancestry of Ae. albopictus mosquitoes from the ancestral and derived regions.

Dates of invasion in the different regions are shown in the lower part of the figure.

Fig. 3. Graphical representation of the most-likely scenario of each set of scenarios describing the dynamics of samples within the native and derived areas using ABC methods.

a Analysis 1: Southeast Asia, La Réunion and the Mediterranean invasion. b Analysis 2: The North America invasion. c Analysis 3: The South America Invasion. d The South America Invasion. e Analysis 4: Central American Invasion. f The Central Africa invasion.

Fig. 4. Graphical representation of the influence of K-ancestry on dissemination and transmission efficiencies.

a Dissemination efficiency (n = 443, 13, 498, 0, 256 and 80 for K1–K6, respectively, overall P = 0.003); and b transmission efficiency (n = 401, 52, 424, 0, 203 and 79 for K1–K6, respectively, overall P = 0.0006). Circles represent the adjusted Odds Ratio estimate and the bar its 95% confidence interval obtained from the logistic regression presented in Tables 3 and 4, respectively.

Fig. 5. Geographical representation of the global spread of Ae. albopictus highlighting the co-ancestry of the different derived populations and the dissemination and transmission efficiencies for Chikungunya virus (CHIKV).

ECSA E1-226V: CHIKV strains from East-Central-South African genotype harbouring a valine at position 226 of E1 glycoprotein. ECSA: CHIKV strains from East-Central-South African genotype harbouring an alanine at position 226 of E1 glycoprotein. ASIA: CHIKV strains from Asian genotype.