Patterns of population structure and polymorphic reproductive isolation in Drosophila melanogaster
Authors: Jenn Coughlan 1,2; Andrius Dagilis 1; Antonio Serrato-Capuchina 3; David Peede 4,5; Dean Castillo 6; Brandon Cooper 7; Daniel Matute 1
Affiliations: 1) University of North Carolina @ Chapel Hill; 2) Department of Ecology and Evolutionary Biology, Yale University; 3) Arnold Arboretum, Harvard University; 4) Department of Ecology, Evolution, and Organismal Biology, Brown University; 5) Center for Computational Molecular Biology, Brown University; 6) Biology Department, University of Nebraska, Omaha; 7) Division of Biological Sciences, University of Montana
Keywords: Speciation & hybridization
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. How genetic and phenotypic variation is partitioned across the range of D. melanogaster, particularly in its putative ancestral range in Subtropical Africa, remains unresolved. Here, we assess patterns of population genetic structure, admixture, mate preference, and genetic incompatibility across a global sample of D. melanogaster, including 174 new accessions from remote regions within Subtropical Africa. While almost all Out of Africa genomes correspond to few genetic ancestries, different geographic regions within Africa contain multiple ancestries, with substantial cryptic diversity in Subtropical Africa. Admixture between distinct lineages is prevalent across the range, but admixture rates vary between lineages. We next perform large scale behavioral surveys of flies from Subtropical Africa and find that female mate choice within Subtropical Africa is highly polymorphic and behavioral types are not monophyletic. This suggests either the repeated evolution of strong female mate choice or substantial admixture between mating types. By quantifying branch specific evolution for flies with strong female choice, we find that the genetic architecture of mate choice is highly polygenic, including loci associated with neurological development, behavior, olfactory perception, and learning. By pairing this population genetic survey with transgenic assays, we explicitly test the role of these candidate loci on behavioral phenotypes, adding to a limited list of genes known to contribute to female mate choice. Additionally, we find that many segregating putative incompatibilities likely evolved during or after expansion out of Africa. However, we find that neither female mate choice nor putative incompatibilities can fully explain overall patterns of population genetic structure, and many of these loci introgress freely between geographic ancestry types. This work contributes to our understanding of the evolution of polymorphic reproductive isolation and how it may contribute to patterns of population genetic structure in a key model organism.