Genomic analysis of European Drosophila melanogaster populations on a dense spatial scale reveals longitudinal population structure and continent-wide selection

Genetic variation is the fuel of evolution. However, analyzing dynamics of evolutionary change in natural populations is challenging, genome sequencing of entire populations remains costly and comprehensive sample collection logistically challenging. To tackle this issue and to define relevant spatial and temporal scales of variation for a population genetic model system, the fruit fly Drosophila melanogaster, we have founded the European Drosophila Population Genomics Consortium (DrosEU). Our principal objective is to employ the strengths of this collaborative consortium to extensively sample and sequence natural populations on a continent-wide scale and across distinct timescales. Here we present the first analysis of the first DrosEU pool-sequencing dataset, consisting of 48 population samples collected across the European continent in 2014. The analysis of this comprehensive dataset uncovers novel patterns of variation at multiple levels: genome-wide neutral SNPs, mtDNA haplotypes, inversions and TEs that exhibit previously cryptic longitudinal population structure across the European continent; signatures of selective sweeps shared among the majority of European populations; presumably adaptive clines in inversions; and geographic variation in TEs. Additionally, we document highly variable microbiota among European fruit fly populations and identify several new Drosophila viruses. Our study reveals novel aspects of the population biology of D. melanogaster and illustrates the power of extensive sampling and pooled sequencing of natural populations on a continent-wide scale.