Correlated variation and population differentiation in satellite DNA abundance among lines of Drosophila melanogaster

Abstract

Tandemly repeating satellite DNA elements in heterochromatin occupy a substantial portion of many eukaryotic genomes. Although often characterized as genomic parasites deleterious to the host, they also can be crucial for essential processes such as chromosome segregation. Adding to their interest, satellite DNA elements evolve at high rates; among Drosophila, closely related species often differ drastically in both the types and abundances of satellite repeats. However, due to technical challenges, the evolutionary mechanisms driving this rapid turnover remain unclear. Here we characterize natural variation in simple-sequence repeats of 2-10 bp from inbred Drosophila melanogaster lines derived from multiple populations, using a method we developed called k-Seek that analyzes unassembled Illumina sequence reads. In addition to quantifying all previously described satellite repeats, we identified many novel repeats of low to medium abundance. Many of the repeats show population differentiation, including two that are present in only some populations. Interestingly, the population structure inferred from overall satellite quantities does not recapitulate the expected population relationships based on the demographic history of D. melanogaster. We also find that some satellites of similar sequence composition are correlated across lines, revealing concerted evolution. Moreover, correlated satellites tend to be interspersed with each other, further suggesting that concerted change is partially driven by higher order structure. Surprisingly, we identified negative correlations among some satellites, suggesting antagonistic interactions. Our study demonstrates that current genome assemblies vastly underestimate the complexity, abundance, and variation of highly repetitive satellite DNA and presents approaches to understand their rapid evolutionary divergence.satellite DNA | population differentiation | rapid evolution H eterochromatin occupies a substantial portion of most eukaryotic genomes and contains vast quantities of tandemly repeating, noncoding DNA elements known as satellite DNA. These sequences, along with transposable elements, are often described as selfish elements or genomic parasites, as they can increase their copy numbers irrespective of host fitness (1, 2). Indeed, they can be highly deleterious for the host genome; for example, ectopic recombination between homologous satellite repeats can lead to devastating chromosomal rearrangements (3, 4). Consequently, these elements are mostly sequestered in repressive chromatin environments around the centromeres and telomeres where there is minimal recombination and transcriptional activity. However, paradoxically, repetitive sequences are also crucial components of euchromatic genomes, as they recruit the centromeric histone H3 variant to form centromeres in many species (5, 6), thereby affecting the fidelity of chromosome segregation (7,8).Adding to the perplexity, satellite DNA turns over at remarkably high rates between species (9, 10). In Drosophila mel...

Radical remodeling of the Y chromosome in a recent radiation of malaria mosquitoes

“…Between humans and chimps whose lineages diverged ∼5 Mya, orthologous satellite arrays in the X centromere are collinear and share 93% sequence identity, whereas collinearity declines and sequence conservation drops to 78% between orthologous satellites in Y centromeres (65). Additional evidence of rapid length, structure, and sequence evolution of satellites and ampliconic structures on the Y chromosome has been reported in mice species 1-2 My diverged and mice subspecies separated by only ∼900,000 y (65), between D. melanogaster and D. simulans that split ∼4 Mya (60,66), and among human males worldwide (67). Despite such pervasive remodeling of the Anopheles Y chromosome over short evolutionary distances, a transgene randomly inserted onto the Y chromosome of an An.…”

The house fly Y Chromosome is young and minimally differentiated from its ancient X Chromosome partner

“…We used the k-Seek method to count the abundance of 2-10 mers in the three male and three female aabys sequencing libraries (Wei et al 2014). We normalized the k-mer counts by multiplying the count by the length of the k-mer and dividing by the number of reads in the library.…”

TALE-light imaging reveals maternally guided, H3K9me2/3-independent emergence of functional heterochromatin in Drosophila embryos

“…Different repetitive sequences acquire distinct chromatin features at the MBT Various highly repetitive sequences that occupy >20% of the D. melanogaster genome are almost always heterochromatic and comprise "constitutive heterochromatin" (Wei et al 2014). The appearance of H3K9me2/3 in interphase 14 marks a step in embryonic formation of constitutive heterochromatin.…”