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.

Keywords: Drosophila; experimental evolution; hyperparasitism; invasion dynamics; transposable elements.

Fig. 1.

Theoretical (filled areas) and empirical (symbols) invasion frequencies of Mos1 brought by migrants carrying one to five copies.

Fig. 2.

(A–C) Copy number dynamics of the Mos1 copies when the autonomous element is alone. Bars represent SEs estimated from the qPCR analysis. Graphs differentiate recipient populations with different genetic backgrounds and overlapping curves indicate independent replicates. (A) [$yw$] population with no Mos1 copy. (B) [$y^{+}{w}^{+}$] population with no Mos1 copy. (C) [$y^{+}{w}^{+}$] population containing Mos1 copies. (D–F) Copy number dynamics when the migrant brings both autonomous Mos1 (red) copies and nonautonomous peach (orange) copies. Recipient populations contained one peach copy per genome. Graphs correspond to different migrant categories. (D) Population initiated with one male. (E) Population initiated with one virgin female. (F) Populations initiated with one nonvirgin female.

Fig. 3.

(A) Dynamics of the number of Mos1 and peach copies from the point where the element has invaded the population (>90% of the population carries at least one copy). The representation on the log scale allows the computation of the transposition rate with a linear regression. (B) Estimate and 95% CI of transposition rates (red: Mos1 copies; orange: peach copies). For peach copies, generations posterior to 60 were not considered, because the invasion clearly stops at that point. The very first generations (during which some individuals in the population do not carry the element) were also discarded. (C) Copy number of Mos1 and peach elements per carrying individual during the initial invasion of the element. Dashed lines show the expected number of copies in absence of transposition. The decrease is due to the higher probability of mating with a Mos1-empty fly during the first generation when the population is not completely invaded.