Genomic Signatures of Microgeographic Adaptation in Anopheles coluzzii Across Urban, Rural, and Forested Environments...

Species distributed across heterogeneous environments often evolve locally adapted populations, but understanding how these persist in the presence of homogenizing gene flow remains puzzling. In Gabon, Anopheles coluzzii, a major African malaria mosquito, is found in various ecological settings, including urban areas, remote rural villages, and forested environments away from any human presence. This study investigates the genomic signatures of local adaptation in populations from distinct environments including the urban area of Libreville, and two proximate sites 10 km apart in the La Lopé National Park (LLP), a village and its sylvatic neighbourhood. Whole genome re-sequencing of 96 mosquitoes unveiled 5.9 million high-quality single nucleotide polymorphisms. Coalescent-based demographic analyses suggest an ∼12,000-year-old divergence between Libreville and La Lopé populations, followed by a secondary contact (∼4000 ybp) resulting in asymmetric effective gene flow. The urban population displayed reduced effective size, evidence of inbreeding, and strong selection pressures likely associated to insecticides or pollution present in urban settings, as suggested by the hard selective sweeps detected in genes involved in detoxification and insecticide resistance. In contrast, the two geographically proximate LLP populations showed larger effective sizes, and distinctive selective signals, notably soft-selective sweeps on the standing genetic variation. Although presumably neutral loci failed to discriminate between LLP populations, our findings support that microgeographic adaptation can swiftly emerge through selection on standing genetic variation despite gene flow. This study contributes to the growing understanding of evolution of populations in heterogeneous environments amid ongoing gene flow and how major malaria mosquitoes adapt to humans and its environment.