Double insertion of transposable elements provides a substrate for the evolution of satellite DNA

Abstract

Eukaryotic genomes are replete with repeated sequences in the form of transposable elements (TEs) dispersed across the genome or as satellite arrays, large stretches of tandemly repeated sequences. Many satellites clearly originated as TEs, but it is unclear how mobile genetic parasites can transform into megabase-sized tandem arrays. Comprehensive population genomic sampling is needed to determine the frequency and generative mechanisms of tandem TEs, at all stages from their initial formation to their subsequent expansion and maintenance as satellites. The best available population resources, short-read DNA sequences, are often considered to be of limited utility for analyzing repetitive DNA due to the challenge of mapping individual repeats to unique genomic locations. Here we develop a new pipeline called ConTExt that demonstrates that paired-end Illumina data can be successfully leveraged to identify a wide range of structural variation within repetitive sequence, including tandem elements. By analyzing 85 genomes from five populations of , we discover that TEs commonly form tandem dimers. Our results further suggest that insertion site preference is the major mechanism by which dimers arise and that, consequently, dimers form rapidly during periods of active transposition. This abundance of TE dimers has the potential to provide source material for future expansion into satellite arrays, and we discover one such copy number expansion of the DNA transposon to approximately 16 tandem copies in a single line. The very process that defines TEs-transposition-thus regularly generates sequences from which new satellites can arise.

Rapid evolution at the Drosophila telomere: transposable element dynamics at an intrinsically unstable locus

“…We conclude that the pattern of HTT arrays are not random, and that this likely reflects the mechanism of HeT-A dependence on TAHRE as well as possible specialization of TART versus TAHRE. The three TART-A elements in tandem on the X chromosome telomere, however, share terminal repeats, which is consistent with recombination between the 3' and 5' terminal repeats [55] and the principal mechanism by which TEs with terminal repeats generate tandems in Drosophila [35]. Thus the higher rate of self-adjacency observed for TART may reflect recombination between termini and/or multiple independent insertions.…”

“…We define sequence abundance as the number of nucleotides each HTT family contributes to the genome; this provides an estimate of the total telomere length that reflects both the copy number and the lengths of the HTT insertions. We independently estimate copy number from the junctions we identify with ConTExt [35], which provides a more direct picture of HTT dynamics than does telomere length alone. In brief, ConTExt aligns repeat derived reads to repeat consensus sequences and uses paired-end information to identify the junctions between repeats and neighboring sequence.…”

“…To investigate whether this heightened diversity observed in the HTTs is characteristic of TEs residing within unstable genomic regions, we consider the sequence diversity of the R-elements. However, while R1 also shows high levels of diversity, this is likely driven by the presence of hundreds of tandemly arrayed R1-elements evolving independently of the active elements [35,42]. A cleaner comparison is with R2, which does not form tandem arrays.…”

“…Both the gag and Pol ORFs are interrupted by several nested TE insertions that are present in most (82/85) strains. Tandem TEs indeed can form by multiple, independent insertions at the same locus, but generally constitute a minority of total insertions and often form at strong consensus insertion sites [35]. If these tandem TAHRE elements reflect true non-telomeric insertions, at least two independent TAHRE insertions must have occurred at this locus.…”

“…A clear picture of within-species HTT variation offers the opportunity to understand how these processes play out over shorter timescales where their impacts on HTT evolution can be more clearly distinguished. Here, we leverage available population genomic data and the ConTExt pipeline [35] to comprehensively analyze HTT sequence and copy number polymorphism in the Drosophila Global Diversity Lines (GDL) [36], encompassing nearly ten thousand HTT insertions in 85 strains of Drosophila melanogaster. We compare the HTTs to other TE families, including those that are similarly restricted to unstable genomic loci.…”