Variable Rates of Simple Satellite Gains across the Drosophila Phylogeny

Abstract

Simple satellites are tandemly repeating short DNA motifs that can span megabases in eukaryotic genomes. Because they can cause genomic instability through nonallelic homologous exchange, they are primarily found in the repressive heterochromatin near centromeres and telomeres where recombination is minimal, and on the Y chromosome, where they accumulate as the chromosome degenerates. Interestingly, the types and abundances of simple satellites often vary dramatically between closely related species, suggesting that they turn over rapidly. However, limited sampling has prevented detailed understanding of their evolutionary dynamics. Here, we characterize simple satellites from whole-genome sequences generated from males and females of nine Drosophila species, spanning 40 Ma of evolution. We show that PCR-free library preparation and postsequencing GC-correction better capture satellite quantities than conventional methods. We find that over half of the 207 simple satellites identified are species-specific, consistent with previous descriptions of their rapid evolution. Based on a maximum parsimony framework, we determined that most interspecific differences are due to lineage-specific gains. Simple satellites gained within a species are typically a single mutation away from abundant existing satellites, suggesting that they likely emerge from existing satellites, especially in the genomes of satellite-rich species. Interestingly, unlike most of the other lineages which experience various degrees of gains, the lineage leading up to the satellite-poor D. pseudoobscura and D. persimilis appears to be recalcitrant to gains, providing a counterpoint to the notion that simple satellites are universally rapidly evolving.

High satellite repeat turnover in great apes studied with short- and long-read technologies

“…O ur observations suggest dependencies among the densities of many repeated motifs , and an underlying structure in their distribution in the great apes genomes -which is at least partially dictated by sequence similarity and evolution, stemming from the interspersion of longer satellite arrays with similar motifs. This echoes recent observations made for Drosophila (Wei et al 2014(Wei et al , 2018 and Chlamydomonas reinhardtii (Flynn et al 2018) . Similarly to the pattern observed in Drosophila , in great apes clusters of co-occurring repeats are in part driven by their sequence similarity.…”

“…It was also hypothesized that the composition of the heterochromatin on the Y may differ from that on other chromosomes because of (1) absence of recombination; (2) a potential role of heterochromatin in silencing the Y; and (3) the small effective population size of the Y (Bachtrog 2013;Nei 1970;Charlesworth and Charlesworth 2000) . Consistent with these hypotheses, some Drosophila species ( D. virilis , D. melanogaster , D. simulans , and D. sechellia ) exhibited many Y-enriched or Y-specific satellite repeats (Wei et al 2018). In contrast, other Drosophila species ( D. pseudoobscura and D. persimilis ) have prominent abundance of transposable elements (TE) on the Y (Wei et al 2018) -suggesting that Y chromosome degeneration occurs by satellite repeat accumulation in some species, and TE accumulation in others.…”

“…Consistent with these hypotheses, some Drosophila species ( D. virilis , D. melanogaster , D. simulans , and D. sechellia ) exhibited many Y-enriched or Y-specific satellite repeats (Wei et al 2018). In contrast, other Drosophila species ( D. pseudoobscura and D. persimilis ) have prominent abundance of transposable elements (TE) on the Y (Wei et al 2018) -suggesting that Y chromosome degeneration occurs by satellite repeat accumulation in some species, and TE accumulation in others. These two alternatives can be explored also for the great ape Y chromosomes, once the assemblies that are currently missing become available.…”

“…Several explanations are possible for this unexpected observation, including incomplete lineage sorting (Kronenberg et al 2018) , parallel gains of the same repeats along different lineages, molecular drive, and segregation distortion (reviewed in (Wei et al 2018)). Future studies should examine each of these explanations in detail.…”

“…melanogaster (Tamura et al 2004) . The differences in satellite repeat abundance in nine Drosophila species were proposed to result predominantly from lineage-specific gains accumulated over the past 40 MY of evolution (Wei et al 2018) . Due to its rapid evolutionary turnover, heterochromatin can serve as a species barrier (Yunis and Yasmineh 1971) .…”