Experimental evolution reveals hyperparasitic interactions among transposable elements

Abstract

Transposable elements (TEs) are repeated DNA sequences that can constitute a substantial part of genomes. Studying TEs' activity, interactions, and accumulation dynamics is thus of major interest to understand genome evolution. Here, we describe the transposition dynamics of cut-and-paste mariner elements during experimental (short-and longer-term) evolution in Drosophila melanogaster. Flies with autonomous and nonautonomous mariner copies were introduced in populations containing no active mariner, and TE accumulation was tracked by quantitative PCR for up to 100 generations. Our results demonstrate that (i) active mariner elements are highly invasive and characterized by an elevated transposition rate, confirming their capacity to spread in populations, as predicted by the "selfish-DNA" mechanism; (ii) nonautonomous copies act as parasites of autonomous mariner elements by hijacking the transposition machinery produced by active mariner, which can be considered as a case of hyperparasitism; (iii) this behavior resulted in a failure of active copies to amplify which systematically drove the whole family to extinction in less than 100 generations. This study nicely illustrates how the presence of transposition-competitive variants can deeply impair TE dynamics and gives clues to the extraordinary diversity of TE evolutionary histories observed in genomes.transposable elements | hyperparasitism | Drosophila | experimental evolution | invasion dynamics

Horizontal transfer and evolution of transposable elements in vertebrates

“…At the other end of the spectrum, Jockey elements and DNA transposons present Ka/Ks ratios that are not significantly lower than one (one-sided, one-sample Mann-Whitney tests, p > 5%, Supplementary Table 2), indicating that these TEs diversify within genomes under more relaxed selection than the others. Their replication would predominantly involve transcomplementation, whereby TE copies are transposed by proteins encoded by other copies 52,53 . For Jockey elements, it is difficult to exclude some degree of cis-preference, as our power to detect selection is limited (Supplementary Discussion).…”

Molecular dissection of a natural transposable element invasion

“…Finally, many earlier studies relied on fairly coarse methods for monitoring TEs, so individual TE var-iants could not be distinguished. This is particularly important as nonautonomous TEs, such as internally deleted copies, could have profound effects on the invasion (Black et al 1987;Robillard et al 2016). Even recent work suffers to varying degrees from the same limitations: No natural TE invasion was investigated and the abundance of different TE variants was not considered (Khurana et al 2011;Rozhkov et al 2013;Robillard et al 2016).…”

“…This is particularly important as nonautonomous TEs, such as internally deleted copies, could have profound effects on the invasion (Black et al 1987;Robillard et al 2016). Even recent work suffers to varying degrees from the same limitations: No natural TE invasion was investigated and the abundance of different TE variants was not considered (Khurana et al 2011;Rozhkov et al 2013;Robillard et al 2016). One study did not investigate the role of small RNAs (Robillard et al 2016), whereas another did not follow the invasion over multiple generations (Khurana et al 2011).…”

New Insights on the Evolution of Genome Content: Population Dynamics of Transposable Elements in Flies and Humans

“…They found that hybrids showed at least one order of magnitude higher transposition rates than parental lines for at least three TE families [100]. Robillard et al [102] estimated transposition rates by qPCR in an experimental evolution study in which a TE insertion was introduced in a strain lacking insertions from that particular family [102]. In the first generations after the introduction of the TE insertion, the transposition rate was 0.33-0.45 per copy per generation, while in the following generations, transposition rates were reduced at least one order of magnitude per copy per generation.…”