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

Abstract

Species distributed across heterogeneous environments often evolve locally adapted ecotypes, but understanding of the genetic mechanisms involved in their formation and maintenance in the face of gene flow is incomplete. In Burkina Faso, the major African malaria mosquito Anopheles funestus comprises two strictly sympatric and morphologically indistinguishable yet karyotypically differentiated forms reported to differ in ecology and behavior. However, knowledge of the genetic basis and environmental determinants of An. funestus diversification was impeded by lack of modern genomic resources. Here, we applied deep whole-genome sequencing and analysis to test the hypothesis that these two forms are ecotypes differentially adapted to breeding in natural swamps versus irrigated rice fields. We demonstrate genome-wide differentiation despite extensive microsympatry, synchronicity, and ongoing hybridization. Demographic inference supports a split only ~1,300 y ago, closely following the massive expansion of domesticated African rice cultivation ~1,850 y ago. Regions of highest divergence, concentrated in chromosomal inversions, were under selection during lineage splitting, consistent with local adaptation. The origin of nearly all variations implicated in adaptation, including chromosomal inversions, substantially predates the ecotype split, suggesting that rapid adaptation was fueled mainly by standing genetic variation. Sharp inversion frequency differences likely facilitated adaptive divergence between ecotypes by suppressing recombination between opposing chromosomal orientations of the two ecotypes, while permitting free recombination within the structurally monomorphic rice ecotype. Our results align with growing evidence from diverse taxa that rapid ecological diversification can arise from evolutionarily old structural genetic variants that modify genetic recombination.