Evolution of a mosquito’s hatching behavior to match its human-provided habitat

Abstract

A subspecies of the yellow fever mosquito, Aedes aegypti, has recently evolved to specialize in biting and living alongside humans. It prefers human odor over the odor of nonhuman animals and breeds in human-provided artificial containers rather than the forest tree holes of its ancestors. Here, we report one way this human specialist has adapted to the distinct ecology of human environments. While eggs of the ancestral subspecies rarely hatch in pure water, those of the derived human specialist do so readily. We trace this novel behavior to a shift in how eggs respond to dissolved oxygen, low levels of which may signal food abundance. Moreover, we show that while tree holes are consistently low in dissolved oxygen, artificial containers often have much higher levels. There is thus a concordance between the hatching behavior of each subspecies and the aquatic habitat it uses in the wild. We find this behavioral variation is heritable, with both maternal and zygotic effects. The zygotic effect depends on dissolved oxygen concentration (i.e., a genotype-environment interaction, or G×E), pointing to potential changes in oxygen-sensitive circuits. Together, our results suggest that a shift in hatching response contributed to the pernicious success of this human-specialist mosquito and illustrate how animals may rapidly adapt to human-driven changes in the environment.