Global evolutionary genetics of Aedes aegypti, the dengue and yellow fever mosquito

The mosquito species Aedes aegypti is the principal vector of dengue and yellow fever viruses across the tropics and subtropics worldwide. Dengue fever is on the rise, affecting approximately 50 million people every year, with 40% of the global human population at risk for infection. Populations of the mosquito display an impressive range of phenotypic and genetic variation. The evolutionary history of this species has been profoundly shaped by humans, and most populations across the globe are highly associated with human habitats. However, it has long been hypothesized that the species originated in Africa as a sylvan form breeding in natural water containers (e.g. treeholes) and feeding primarily on non-human animals. Many ecologically similar populations still exist across sub-Saharan Africa, and are known as the subspecies Aedes aegypti formosus. The more common, highly human-associated subspecies, Aedes aegypti aegypti, is thought to have evolved from such ancestral forest forms through adaptations to human habitats, and spread with human movement across the global tropics. In recent years, an increasing number of human-associated Ae. aegypti populations have been identified in Africa, where the true domestic form, Ae. ae. aegypti was believed absent. This raised the question as to whether these populations represent independent incursions of Ae. ae. formosus into human habitats, or are evolutionarily related to domestic populations (Ae. ae. aegypti) from other areas of the world.;In this dissertation work, I used presumed neutral genetic markers (microsatellites, sequenced nuclear loci, and SNPs) to 1) examine genetic structure in the species and test whether geographically, ecologically, and temporally distinct populations of Ae. aegypti are also genetically distinct, and 2) determine the evolutionary history of the species, including the emergence of ecological phenotypes and domesticity. Results of population genetic analyses showed the two subspecies of Ae. aegypti to be genetically distinct, and though populations of Ae. ae. formosus across Africa did not show much structuring, high levels of genetic structure were found between populations within the pantropical domestic subspecies Ae. ae. aegypti (Chapters 1 and 4). Because of this, I was able to clearly assign individual pantropical mosquitoes back to their population of origin, an ability that was used in Chapter 2 to determine that a recent introduction of Ae. aegypti in the Netherlands originated from a tire shipment out of Miami, Florida. In contrast, genetic structuring was largely absent across temporally distinct populations: those collected several years apart from the same location. However, this pattern varied by collection site (Chapter 3).;Phylogenetic and population genetic analyses of global Ae. aegypti populations support the hypothesis that the species originated in Africa as a form similar to Ae. ae. formosus, from which the domestic subspecies evolved and spread to the New World, followed by the Asia-Pacific region (Chapters 1 and 4). Two patterns strongly support this conclusion: (a) sub-Saharan African samples show considerably greater genetic variation, especially with regard to the number of alleles present and (b) phylogenetic analyses indicate the African populations are basal, i.e., are subtended by the deepest branches in the overall tree. However, human-associated populations in Africa appear to be the result of independent incursions of the species into human habitats, as they are genetically identified as Ae. ae. formosus, and evolutionarily distinct from the domestic subspecies Ae. ae. aegypti. This suggests that the species has the propensity to continue invading human habitats across the African landscape, leading to increased opportunities for epidemic disease spread. Overall, the studies performed during the course of my dissertation research indicate that humans have profoundly affected genetic diversity in Ae. aegypti and have shaped the evolutionary history of the species. These evolutionary patterns may be relevant in other disease vector systems, as well as in a multitude of invasive species with close ecological interactions with humans.