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

Abstract

Background: Drosophila telomeres have been maintained by three families of active transposable elements (TEs), HeT-A, TAHRE and TART, collectively referred to as HTTs, for tens of millions of years.The conservation of this arrangement contrasts with an unusually high degree of HTT interspecific variation. While the impacts of conflict and domestication are often invoked to explain HTT variation, the telomeres are unstable structures such that neutral mutational processes and evolutionary tradeoffs may also drive HTT evolution. Results:We leveraged population genomic data to analyze nearly 10,000 HTT insertions in 85 D.melanogaster genomes and compared their variation to TE families evolving under more typical dynamics. We find that distinct aspects of HTT copy number variation and sequence diversity largely reflect telomere instability, with HTT insertions being lost at much higher rates than other TEs elsewhere in the genome. However, occasional copy number expansions of both HTTs and other TE families occur, highlighting that the HTTs are, like their feral cousins, typically repressed but primed to take over given the opportunity. We further find that some HTT families may be activated by the erosion of whole telomeres, suggesting the existence of HTT-specific host control mechanisms. Conclusions:Even the persistent telomere localization of HTTs may not reflect domestication, but rather a highly successful evolutionary strategy to reduce their impact on the host genome. We propose that HTT evolution is driven by multiple processes including domestication, genetic conflict, niche specialization, and telomere instability, with the latter two being previously underappreciated and likely predominant.

Silence at the End: How Drosophila Regulates Expression and Transposition of Telomeric Retroelements

“…Studies carried out in flies bearing TDs as well as in somatic cells revealed that transposition events are regulated at different levels and involve distinct classes of regulators: a) cis-acting factors b) telomere capping proteins c) chromatin factors d) DNA repair proteins and e) still-uncharacterized genetic factors. The evidence that the majority of regulators are factors that are not encoded by telomeric retroelements supports the view of a host-transposon mutualisticinteraction that reduces the cost to the host of transposon activity[17,61,62]…”

“…Finally, the acquisition of Het-A, TART and TAHRE at telomeres of mitotic chromosomes might rely more on recombination and/or gene conversion events rather than on transposition. Both events indeed account for telomere healing and de novo telomere formation that frequently occur in natural populations [60,61], which underscore their importance in telomere maintenance. It is worth noting that recombination between chromosome end sequences is at the base of the Alternative Lengthening of Telomeres (ALT) pathway that a subset of cancers uses to elongate their telomeres in order to prevent the telomere shortening normally occurring in proliferating cells [138].…”

“…H3K9me3 residues recruit Rhino, which favors production of telomeric piRNAs, and concomitantly HP1a forms repressive chromatin domains [91]. Since Drosophila telomeres are 50 kbp long on average [61], the two chromatin patterns might occupy different parts of the HTT array.…”

“…The 5' end of the most distal element is located at the extremity of the chromosome and may thus be subjected to terminal erosion until a new element is added onto the end. Only 20% of the Het-A or TAHRE insertions and 7% of the TART insertions are represented by full-length elements[38,61].…”

Identifying the causes and consequences of assembly gaps using a multiplatform genome assembly of a bird‐of‐paradise

“…More generally, repetitive elements can play important roles in many molecular and cellular mechanisms, and as a source of genetic variability (Bourque et al., 2018). They have contributed to evolutionary novelty in many organismal groups, by giving rise to important evolutionary features such as the mammalian placenta (Emera & Wagner, 2012), the vertebrate adaptive immune system (Kapitonov & Koonin, 2015; Zhang et al., 2019) and other telomere repair systems (Levis et al., 1993; McGurk et al., 2019). Thus, having genome assemblies that are as complete as possible facilitates research into a multitude of molecular phenomena (Slotkin, 2018).…”