Genetic divergence in Aedes aegypti mosquitoes potentially associated with enhanced capacity for arbovirus transmission

Abstract

Aedes aegypti is the most important mosquito vector of arboviruses worldwide, originating on islands of the southwest Indian Ocean before spreading to Africa and, more recently, the Americas and Asia. Migration out of Africa was enabled by the evolution of behaviors that increased human-vector contact, and as Ae. aegypti became more domesticated, arboviral competence may have also increased. Here we investigate variation in vector competence between present-day populations of Ae. aegypti from Florida (USA) and Tanzania (East Africa) and use a genomics approach to examine genetic differentiation potentially underlying traits important for arbovirus transmission. Using vector-competence experiments with dengue virus serotype 2, we demonstrate greater susceptibility to infection in American mosquitoes, along with higher viral loads and a shorter time to virus dissemination. We then sought to identify highly divergent genes potentially underlying these differences and discovered more than 1.6 million single nucleotide polymorphisms via exome sequencing. Of these, 1058 were highly differentiated between populations (F ST > 0.9) with more than half mapping to 17 outlier genes influencing chromatin remodeling, lipid metabolism, glycosylation, circadian rhythms, olfaction, and saliva bioactivity. Eight of these outlier genes formed a highly divergent genomic island on chromosome 2. Allele-frequency patterns of outlier genes across Ae. aegypti ’s range highlight genetic differentiation within sub-Saharan Africa, as well as evolutionary changes accompanying the shift towards domestication in the Americas and Asia. This work offers insights into phenotypic variation and evolutionary divergence within Ae. aegypti , including naturally occurring genetic variants that may influence transmission-related characters.