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Genetic variation is the fuel of evolution but analysing the spatio-temporal dynamics of genetic changes in natural populations is challenging, comprehensive sampling logistically difficult, and sequencing of entire populations costly. Here we address these issues by performing the first continent-wide genomic analysis of genetic variation in European Drosophila melanogaster , based on 48 pool-sequencing samples from 32 populations. Our analyses uncover a novel pattern of major longitudinal population structure; establish previously unknown clines in inversions and transposable elements across Europe; and provide evidence for non-local, continent-wide selective sweeps that are shared among the majority of populations. We also find pronounced variation among populations in the composition of the fly microbiome and identify five new DNA viruses adding to a single example known so far for this species. Our study has important implications for the evolution and demography of D. melanogaster , an ancestrally African species that first colonized Europe before becoming cosmopolitan.

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