Horizontal transfer and evolution of transposable elements in vertebrates

Hua-Hao Zhang,Min-Rui-Xuan Xu,Xiao-Gu Zhang,Jean Peccoud,Clément Gilbert

doi:10.1038/s41467-020-15149-4

Abstract

Horizontal transfer of transposable elements (HTT) is an important process shaping eukaryote genomes, yet very few studies have quantified this phenomenon on a large scale or have evaluated the selective constraints acting on transposable elements (TEs) during vertical and horizontal transmission. Here we screen 307 vertebrate genomes and infer a minimum of 975 independent HTT events between lineages that diverged more than 120 million years ago. HTT distribution greatly differs from null expectations, with 93.7% of these transfers involving ray-finned fishes and less than 3% involving mammals and birds. HTT incurs purifying selection (conserved protein evolution) on all TEs, confirming that producing functional transposition proteins is required for a TE to invade new genomes. In the absence of HTT, DNA transposons appear to evolve neutrally within genomes, unlike most retrotransposons, which evolve under purifying selection. This selection regime indicates that proteins of most retrotransposon families tend to process their own encoding RNA (cis-preference), which helps retrotransposons to persist within host lineages over long time periods.

Highlights

Horizontal transfer of transposable elements (HTT) is an important process shaping eukaryote genomes, yet very few studies have quantified this phenomenon on a large scale or have evaluated the selective constraints acting on transposable elements (TEs) during vertical and horizontal transmission
We investigated HTT involving most TE types among 307 vertebrate species whose genome sequences are publicly available on GenBank (Supplementary Data 1), following principles developed in earlier studies[18,24]
To conclude, our study reveals that the evolutionary history of TEs in vertebrates has been punctuated by a large number of horizontal transfer (HT) events, most of which involved members of the Tc1/Mariner superfamily in ray-finned fishes

Summary

Introduction

Horizontal transfer of transposable elements (HTT) is an important process shaping eukaryote genomes, yet very few studies have quantified this phenomenon on a large scale or have evaluated the selective constraints acting on transposable elements (TEs) during vertical and horizontal transmission. In the absence of HTT, DNA transposons appear to evolve neutrally within genomes, unlike most retrotransposons, which evolve under purifying selection. This selection regime indicates that proteins of most retrotransposon families tend to process their own encoding RNA (cispreference), which helps retrotransposons to persist within host lineages over long time periods. We leverage our HTT detection pipeline to unveil broad-scale patterns of selection acting on DNA transposons and retrotransposons during both transposition within host lineages and horizontal transfer. Most retrotransposons diversify within genomes under purifying selection, which suggests that retrotransposon proteins tend to preferentially process and reverse transcribe their own encoding RNAs

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Conclusion