Experimental evolution reveals hyperparasitic interactions among transposable elements

Émilie Robillard,Arnaud Le Rouzic,Zheng Zhang,Pierre Capy,Aurélie Hua-Van

doi:10.1073/pnas.1524143113

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.

Highlights

The evolutionary factors explaining the distribution of transposable elements (TEs) across organisms are still poorly understood [1]
It has been recently suggested that the relationships between genome components were similar to the relationships between individuals or species in ecosystems [10, 49, 50], the possibility to apply ecological formalism to genome evolution remains questionable [51]
As active transposable elements themselves are often considered as parasites of the genome [52, 53], this genome-ecology analogy would define nonautonomous copies as hyperparasites

Summary

Introduction

The evolutionary factors explaining the distribution of transposable elements (TEs) across organisms are still poorly understood [1]. TEs are mobile DNA sequences able to invade populations and to duplicate within genomes by various molecular mechanisms [2] and can be found in multiple copies in virtually all living species. Whatever the molecular mechanism (e.g., copy-and-paste or cut-and-paste), transposition requires the production of one or several proteins encoded by the TE itself [11] These proteins may promote the amplification of any similar copies, including those that do not produce any functional transposition machinery. Two distinct mariner sequences have been isolated from Drosophila mauritiana, a sister species of Drosophila melanogaster [19, 20] Both copies are full-length, but one (peach) is nonautonomous, unable to promote its own transposition due to nonsynonymous substitutions, whereas the other (Mos1) is an autonomous copy able to cross-mobilize peach copies. We used the mariner system in D. melanogaster through two series of experiments to study the capacity of Mos1-active

Methods

Results

Discussion

Conclusion