Dating the origin and spread of specialization on human hosts in Aedes aegypti mosquitoes

The globally invasive mosquito subspecies Aedes aegypti aegypti is a
highly effective vector of human arboviruses because it specializes in
biting humans and breeding in human habitats. Recent work suggests that
specialization first arose as an adaptation to long, hot dry seasons in
the West African Sahel, where Ae. aegypti is forced to rely on
human-stored water for breeding. However, rainfall patterns in this region
have changed dramatically over the past 10–20 thousand years, and we do
not yet know exactly when specialization occurred. Here we use
whole-genome cross-coalescent analysis to date the emergence of human
specialist populations in the Sahel and thus further probe the climate
hypothesis. Importantly, we take advantage of the known migration of
human-specialist populations out of Africa during the Atlantic Slave Trade
to calibrate the coalescent clock and thus obtain a more precise estimate
of the older evolutionary event than would otherwise be possible. We find
that human-specialist mosquitoes diverged rapidly from ecological
generalists approximately 5,000 years ago, which corresponds to the end of
the African Humid Period—a time when the Sahara dried and water stored by
humans became a uniquely stable, aquatic niche in the Sahel. We also use
population genomic analyses to date a previously observed influx of
human-specialist alleles into major West African cities, where mosquitoes
tend to be more attracted to humans than in nearby rural populations
regardless of climate. In this case, the characteristic length of tracts
of human-specialist ancestry present on a generalist genetic background in
Kumasi, Ghana and Ouagadougou, Burkina Faso suggests the change in
behavior occurred during rapid urbanization over the last 20–40 years.
Taken together, we show that the timing and ecological context of two
previously observed shifts toward human biting in Ae. aegypti differ;
climate was likely the original driver, but urbanization has become
increasingly important in recent decades. Understanding the changing
relationship between mosquitoes and humans over time is critical for
predicting and managing the burdens of mosquito-borne disease.