Population structure and introgression among recently differentiated Drosophila melanogaster populations

Understanding the factors that produce and maintain genetic variation is a central goal of evolutionary biology. Despite a century of genetic analysis, the evolutionary history underlying patterns of exceptional genetic and phenotypic variation in the model organism Drosophila melanogaster remains poorly understood. In particular, how genetic and phenotypic variation is partitioned across global D. melanogaster populations, and specifically in its putative ancestral range in Subtropical Africa, remains unresolved. Here, we integrate genomic and behavioral analyses to assess patterns of population genetic structure, admixture, mate preference, and genetic incompatibility throughout the range of this model organism. Our analysis includes 174 new accessions from novel and under-sampled regions within Subtropical Africa. We find that while almost all Out of Africa genomes correspond to a single genetic ancestry, different geographic regions within Africa contain multiple distinct ancestries, including the presence of substantial cryptic diversity within Subtropical Africa. We find evidence for significant admixture--and variation in admixture rates--between geographic regions within Africa, as well as between African and non-African lineages. By combining behavioral analysis with population genomics, we demonstrate that female mate choice is highly polymorphic, behavioral types are not monophyletic, and that genomic differences between behavioral types correspond to many regions across the genome. These include regions associated with neurological development, behavior, olfactory perception, and learning. Finally, we discovered that many individual pairs of putative incompatibility loci likely evolved during or after the expansion of D. melanogaster out of Africa. This work contributes to our understanding of the evolutionary history of a key model system, and provides insight into the distribution of reproductive barriers that are polymorphic within species.