Dynamic evolution of euchromatic satellites on the X chromosome in Drosophila melanogaster and the simulans clade

Repeats are abundant in eukaryotic genomes and contribute to differences in genome size and organization among organisms. The large blocks of tandem repeats--satellite DNAs (satDNAs)--frequently found in regions of low recombination can turn over rapidly between species, with potential consequences for genome evolution and speciation. Short blocks of satDNA also exist in the euchromatin, where they are particularly abundant on the X chromosome. These euchromatic repeats can affect gene expression and some have roles dosage compensation. Despite their abundance and impact on important phenotypes, we know little about the detailed evolutionary dynamics and the processes that shape satDNA distributions in genomes over short evolutionary time scales. Here we use high-quality genome assemblies to study the evolutionary dynamics of satDNA across closely related species: Drosophila melanogaster and three species of the simulans clade (D. simulans, D. sechellia, and D. mauritiana). We focus on two complex satDNA families, Rsp-like and 1.688 gm/cm3. These repeats are highly dynamic in the heterochromatin, where their genomic location varies. We discovered that euchromatic repeats are similarly dynamic, changing in abundance, number of clusters, and composition within clusters, even across the simulans clade. While 1.688 is an old repeat family, Rsp-like has recently proliferated, spreading to new genomic locations across the X chromosome independently in D. simulans and D. mauritiana. We infer that extrachromosomal circular DNA integration and/or interlocus gene conversions resolved by microhomology-mediated repair pathways could account for satDNA proliferation in genomes. The divergence of repeat landscapes between species may have important consequences for genome evolution.