Variation in spatial population structure in theAnopheles gambiaespecies complex

Abstract

AbstractAnopheles gambiae, Anopheles coluzzii, andAnopheles arabiensisare three of the most widespread vectors of malaria parasites, with geographical ranges stretching across wide swaths of Africa. Understanding the population structure of these closely related species, including the extent to which populations are connected by gene flow, is essential for understanding how vector control implemented in one location might indirectly affect vector populations in other locations. Here, we assessed the population structure of each species based on whole-genome sequences from the third phase of theAnopheles gambiae1000 Genomes Project. The data set included single nucleotide polymorphisms from whole genomes of 2,242 individual mosquitoes sampled from 119 locations across 19 African countries. We found thatA. gambiaesampled from several countries in West and Central Africa showed low genetic differentiation from each other according to principal components analysis (PCA) and ADMIXTURE modeling. Using Estimated Effective Migration Surfaces (EEMS), we showed that this low genetic differentiation indicates high effective migration rates forA. gambiaeacross this region. Outside of this region, we found six groups of sampling locations from Central, East, and Southern Africa for whichA. gambiaeshowed higher genetic differentiation, and lower effective migration rates, between each other and the West/Central Africa group. These results indicate that the barriers to and corridors for migration between populations ofA. gambiaediffer across the geographical range of this malaria vector species. Using the same methods, we found higher genetic differentiation and lower migration rates between populations ofA. coluzziiin West and Central Africa than forA. gambiaein the same region. On the other hand, we found lower genetic differentiation and higher migration rates between populations ofA. arabiensisin Tanzania, compared toA. gambiaein the same region. These differences betweenA. gambiae, A. coluzzii, andA. arabiensisindicate that migration barriers and corridors may vary between species, even for very closely related species. Overall, our results demonstrate that migration rates vary both between and within species ofAnophelesmosquitoes, presumably based on species-specific responses to the ecological or environmental conditions that may impede or facilitate migration, and the geographical patterns of these conditions across the landscape. Together with previous findings, this study provides robust evidence that migration rates between populations of malaria vectors depend on the ecological context, which should be considered when planning surveillance of vector populations, monitoring for insecticide resistance, and evaluating interventions.