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Female mosquitoes are major vectors of human disease and the most dangerous are those that preferentially bite humans. A 'domestic' form of the mosquito Aedes aegypti has evolved to specialize in biting humans and is the main worldwide vector of dengue, yellow fever, and chikungunya viruses. The domestic form coexists with an ancestral, 'forest' form that prefers to bite non-human animals and is found along the coast of Kenya. We collected the two forms, established laboratory colonies, and document striking divergence in preference for human versus non-human animal odour. We further show that the evolution of preference for human odour in domestic mosquitoes is tightly linked to increases in the expression and ligand-sensitivity of the odorant receptor AaegOr4, which we found recognizes a compound present at high levels in human odour. Our results provide a rare example of a gene contributing to behavioural evolution and provide insight into how disease-vectoring mosquitoes came to specialize on humans.
Blood-feeding as a behavioural adaptation is exceedingly rare in insects. Of the one million to ten million insect species on earth, only ~ 10,000 feed on the blood of live animals1. Among these, only about 100 species blood-feed preferentially on humans1. When biting insects evolve to prefer humans, they can spread diseases such as malaria and dengue fever with devastating efficiency. The mosquito Aedes aegypti provides one of the best examples of specialization on humans. It originated as a wild, animal-biting species in the forested areas of sub-Saharan Africa, where the subspecies Ae. aegypti formosus is still often found living in forests and biting non-human animals today2 4. In contrast, the derived non-African subspecies Ae. aegypti aegypti has evolved to specialize in biting humans and thus has become the main worldwide vector of dengue and yellow fevers2(TM)4.
The evolutionary adaptations that help subspecies Ae. aegypti aegypti exploit humans are most clearly seen where it has been reintroduced along the coast of East Africa and is known as the 'domestic' form. Researchers investigating the outbreak of an unknown illness in Tanganyika in 1952 discovered homes heavily populated by brown-pigmented 'domestic' mosquitoes5. Subsequent work in the Rabai region of Kenya in the 1960s and 1970s showed that domestic mosquitoes readily entered homes6, preferred to lay eggs in nutrient-poor river and...