Evolutionary dynamics of simple sequence repeats across long evolutionary time scale in genus Drosophila

Repetitive DNA is among the fastest evolving types of genomic DNA, which includes simple sequence repeats (SSRs), short regions of tandemly repeated one to six nucleotides long motifs. SSRs are found most frequently in noncoding regions. Repeat number variation occurs rapidly and is presumably neutral such that polymorphic SSRs are frequently used as genetic markers to characterize and classify populations. Despite their rapid evolution, recent reports suggested that SSR loci can be retained over hundreds of millions of years. We here investigate the dynamics and genomic features of SSR evolution in syntenic regions conserved across twelve Drosophila species and within a D. melanogaster population dataset. We find that SSR loci decay exponentially with time, the percentage of retained SSRs mostly reflects species relationships and correlates well with the sequence similarity of neighboring genes. About 47% of repeat loci within syntenic regions may share common ancestry due to predicted conservation in at least two species from the Drosophila subgenera Sophophora and Drosophila respectively, i.e. after 80 million years of divergence time. Since loci which are highly polymorphic at the population level also decay faster across species, SSR evolution appears to be a gradual process in which conservation pressure may act at relatively constant rates across time scales. A higher proportion of SSR loci are retained among Drosophila subgenus species considering their evolutionary distance and the expected decay rate estimated across all Drosophila species. This prolonged SSR retention might be caused by a higher SSR mutation rate and a lower nucleotide substitution rate in the Drosophila subgenus compared to Sophophora species. SSRs in exons and on autosomes evolve more slowly than SSRs located outside of exons or on the sex chromosome, respectively, both within and across species. SSR variability and phylogenetic conservation thus varies depending on the genomic location. These findings provide new insights into the dynamics of SSRs at both micro- and macro-evolutionary scales. The development of robust models of SSR long-term evolution will facilitate more in-depth analyses in general and the prediction of neutrally evolving SSRs and SSRs evolving under purifying selection, extending our knowledge of the functional impact of SSRs in genome evolution.