Tracking adaptive evolution in real time in an invasive fruit fly

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PROJECT SUMMARY Invasive species, which can carry diseases, decimate food crops and threaten biodiversity, are immensely successful in new environments, but the biological mechanisms that enable their spread remain elusive. Some invasive species show signs of rapid adaptation to new habitats, but few studies have captured post-invasion adaptation in real time. Additionally, invasive species colonizing multiple habitats simultaneously offer the opportunity to study the longstanding question of whether evolution is predictable. To understand how quickly and predictably organisms adapt to newly colonized environments, detailed genomic studies of repeated incipient invasions are necessary. In this study, we will genetically and phenotypically characterize North American populations of the African Fig Fly, Zaprionus indianus, to test for local adaptation and parallel evolution in its ongoing invasion. This tractable model organism arrived in North America less than two decades ago and rapidly spread. Our data suggest it is locally extirpated from temperate habitats each winter and re-colonizes these locales each spring. Our central hypothesis is that Z. indianus undergoes predictable post-colonization adaptation across multiple locations and years, resulting in repeated changes in allele frequencies and ecologically relevant phenotypes. To test this hypothesis, we will collect, sequence, and phenotype isolates from along the East Coast of North America and from two focal Virginia orchards over multiple years. In Aim 1, we will quantify genetic and phenotypic variation in North American populations by generating pooled sequencing of populations collected along a latitudinal gradient to test for clinally varying polymorphisms over two sampling years. We will also phenotype lines collected at different latitudes to test for clinal differences in morphological, life-history, and stress tolerance phenotypes. Repeated clinal and phenotypic differentiation would present evidence for rapid adaptation to local environments. In Aim 2, we will sample and sequence flies from two geographically separate Virginia orchards over three growing seasons to test for alleles and phenotypes that predictably change following invasion. These experiments will allow us to identify the genomic targets of post-invasion adaptation and quantify the predictability of evolution. In Aim 3, we will characterize the putative target of a recent selective sweep in North American flies: a 600 kb haplotype that is common in Virginia, intermediate frequency in Florida, and not found in Africa. We will generate outbred populations fixed for alternate alleles and perform RNAseq to test for differential gene expression associated with alternate haplotypes. Phenotyping experiments will explore the potential functional targets of this sweep, allowing us to dissect the biological function of a genomic signal of selection. Collectively, these experiments will take a multipronged approach to test for post-invasion adaptation and parallel evolution in real time. This study will provide a framework to understanding rapid adaptation to novel environments and predicting evolutionary trajectories of future invasive species, which may lead to solutions to control their spread.