Wild origin of Anopheles gambiae – WILDING

Since its discovery at the beginning of the twentieth century, Anopheles gambiae has amazed and challenged the scientific community by its ability to be virtually everywhere in sub-Saharan Africa. This adaptation has been driven by its close relation to humans, who provide blood meals, shelters, and breeding sites. In return, An. gambiae transmits malaria in remote villages as in larges cities across the continent. Therefore, understanding the origin and the mechanisms underlying human adaptation of the malaria vector Anopheles gambiae is decisive for the successful control of malaria in Africa. During an exploratory survey at La Lopé National Park (Gabon) in 2014, we morphologically identified the mosquito An. gambiae in several remote wild locations, far away from any human activity or presence. This observation has shaken the foundations of our historical beliefs about the ecology of this vector, that is, An. gambiae is strictly confined to anthropogenic habitats. Subsequent fieldwork studies and preliminary molecular analysis confirmed the stable presence of two members of the An. gambiae complex, An. gambiae and An. coluzzii, in sylvatic (park) and domestic (village, at 15 km away) settings, An. coluzzii being the predominant species in both habitats. Besides that both mosquitoes species need to feed on animals in the park, they still maintained their ability to feed on humans. Ongoing genomics analysis of sylvatic and domestic An. coluzzii populations encouraged our library construction and sequencing strategy to detect heterozygous variants between the two populations. Although we presume a process of local adaptation (i.e., back to the ancestral wild status from domestic populations by recently derived genetic changes in its ecology, feeding and biting behavior), currently, it is impossible to properly say whether the presence of both mosquitoes in wild habitats represents an ancestral wild taxon. Our main objective is to understand the origin and evolution of adaptive traits of wild populations of An. gambiae and An. coluzzii. To this aim, we will carry out an extensive fieldwork at La Lopé National Park (park and village) and in two other sites of Gabon, following an anthropogenic gradient. Our experimented sampling design, including different kinds of traps and behavioral tests, will elucidate the ecological (population dynamics, breeding sites, seasonality) and behavioral (host preference, biting time, feeding behavior) traits associated to sylvatic vs. domestic populations. Then, following our genomic approach, we will dissect the genetic basis of the origin and the evolution of sylvatic populations, and consequently, specialization to humans. Overall, our outcomes will have a direct impact on malaria control. First, we will understand whether conventional control strategies (i.e. indoor insecticide spray) may affect the exposure and susceptibility of wild living populations of An. gambiae and An. coluzzii, and, the epidemiological risk for human populations living at the edge of natural areas. And second, we will investigate the genetic basis of human adaptation (i.e. host preference), which in turn, may be used for new genetic vector control strategies (i.e. zooprophilaxis). Finally, the outcomes of this exploratory project will allow the coordinator to pursue this new and original research area in a broader study with the submission of an ERC research grant on how to predict evolution of malaria vectors facing anthropogenic pressures.