Standing genetic variation and chromosome differences drove rapid ecotype formation in a major malaria vector

Local adaptation results in the formation of ecotypes—conspecific groups with heritable differences that increase fitness to distinct environments. The adaptive significance of ecotypes is widely recognized, but not its genetic basis. Here, focusing on a dominant pan-African malaria vector, we study two co-occurring isomorphic yet karyotypically differentiated populations from Burkina Faso reported to differ in larval ecology and epidemiologically relevant adult behaviors. Since their discovery in the 1990s, further investigation was precluded by lack of modern genomic resources. Here, we used deep whole-genome sequencing and analysis to test the hypothesis that these two morphologically cryptic groups are ecotypes differentially adapted to breeding in natural swamps versus irrigated rice fields. We conclusively demonstrate genome-wide differentiation despite extensive microsympatry, synchronicity, and occasional hybridization. Demographic inference supports a split only ~1,300 years ago, coinciding with the massive expansion of domesticated African rice cultivation, suggesting that a newly abundant anthropogenic habitat may have driven vector diversification. The genomic pattern of differentiation is heterogenous, and we infer that the regions of highest differentiation were under selection during lineage splitting, consistent with local adaptation. The origin of nearly all variation implicated in local adaptation, including chromosomal inversions, substantially predates the ecotype split, suggesting that rapid adaptation to rice fields was fueled mainly by standing genetic variation. Sharp differences in chromosomal inversion polymorphism between ecotypes likely promoted adaptive divergence, by maximizing recombination within the homokaryotypic standard rice ecotype, and suppressing admixture with the other ecotype, which carries inverted arrangements at high frequencies.