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The population genetic perspective is that the processes shaping genomic variation can be revealed only through simultaneous investigation of sequence polymorphism and divergence within and between closely related species. Here we present a population genetic analysis of Drosophila simulans based on whole-genome shotgun sequencing of multiple inbred lines and comparison of the resulting data to genome assemblies of the closely related species, D. melanogaster and D. yakuba. We discovered previously unknown, large-scale fluctuations of polymorphism and divergence along chromosome arms, and significantly less polymorphism and faster divergence on the X chromosome. We generated a comprehensive list of functional elements in the D. simulans genome influenced by adaptive evolution. Finally, we characterized genomic patterns of base composition for coding and noncoding sequence. These results suggest several new hypotheses regarding the genetic and biological mechanisms controlling polymorphism and divergence across the Drosophila genome, and provide a rich resource for the investigation of adaptive evolution and functional variation in D. simulans.
Population genomics, the study of genome-wide patterns of sequence variation within and between closely related species, can provide a comprehensive view of the relative importance of mutation, recombination, natural selection, and genetic drift in evolution. It can also provide fundamental insights into the biological attributes of organisms that are specifically shaped by adaptive evolution. One approach for generating population genomic datasets is to align DNA sequences from whole-genome shotgun projects to a standard reference sequence. We used this approach to carry out whole-genome analysis of polymorphism and divergence in Drosophila simulans, a close relative of the model system, D. melanogaster. We find that polymorphism and divergence fluctuate on a large scale across the genome and that these fluctuations are probably explained by natural selection rather than by variation in mutation rates. Our analysis suggests that adaptive protein evolution is common and is often related to biological processes that may be associated with gene expression, chromosome biology, and reproduction. The approaches presented here will have broad applicability to future analysis of population genomic variation in other systems, including humans.
Low-coverage genome sequences from multiple Drosophila simulans strains provide the first comprehensive view of polymorphism and divergence in the fruit fly.