Experimental evolution reveals hyperparasitic interactions among transposable elements

• Published in: Proceedings of the National Academy of Sciences - PNAS Vol. 113; no. 51; pp. 14763 - 14768
• Main Authors: Robillard, Émilie, Le Rouzic, Arnaud, Zhang, Zheng, Capy, Pierre, Hua-Van, Aurélie
• Format: Journal Article
• Language: English
• Published: United States National Academy of Sciences 20.12.2016
• Subjects: Animals; Biological Sciences; Deoxyribonucleic acid; Directed Molecular Evolution; DNA; DNA Transposable Elements; DNA-Binding Proteins - genetics; Drosophila melanogaster - genetics; Extinction; Female; Genome, Insect; Genomes; Insects; Linear Models; Male; Parasites; Phenotype; Phylogeny; Polymerase Chain Reaction; Species Specificity; Transposases - genetics; experimental evolution; hyperparasitism; invasion dynamics; transposable elements; Drosophila
• ISSN: 0027-8424; 1091-6490
• DOI: 10.1073/pnas.1524143113

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.