Massive horizontal transfer of transposable elements in insects
Jean Peccouda,1, Vincent Loiseaua, Richard Cordauxa, and Clément Gilberta,1
Author Affiliations
Edited by Nancy L. Craig, Johns Hopkins University School of Medicine, Baltimore, MD, and approved March 20, 2017 (received for review December 22, 2016)
Significance
Eukaryotes normally receive their genetic material from their parents but may occasionally, like prokaryotes do, acquire DNA from unrelated organisms through horizontal transfer (HT). In animals and plants, HT mostly concerns transposable elements (TEs), probably because these pieces of DNA can move within genomes. Assessing the impact of HTs on eukaryote evolution and the factors shaping the dynamics of these HTs requires large-scale systematic studies. We have analyzed the genomes from 195 insect species and found that no fewer than 2,248 events of HT of TEs occurred during the last 10 My, particularly between insects that were closely related and geographically close. These results suggest that HT of TEs plays a major role in insect genome evolution.
Abstract
Horizontal transfer (HT) of genetic material is central to the architecture and evolution of prokaryote genomes. Within eukaryotes, the majority of HTs reported so far are transfers of transposable elements (TEs). These reports essentially come from studies focusing on specific lineages or types of TEs. Because of the lack of large-scale survey, the amount and impact of HT of TEs (HTT) in eukaryote evolution, as well as the trends and factors shaping these transfers, are poorly known. Here, we report a comprehensive analysis of HTT in 195 insect genomes, representing 123 genera and 13 of the 28 insect orders. We found that these insects were involved in at least 2,248 HTT events that essentially occurred during the last 10 My. We show that DNA transposons transfer horizontally more often than retrotransposons, and unveil phylogenetic relatedness and geographical proximity as major factors facilitating HTT in insects. Even though our study is restricted to a small fraction of insect biodiversity and to a recent evolutionary timeframe, the TEs we found to be horizontally transferred generated up to 24% (2.08% on average) of all nucleotides of insect genomes. Together, our results establish HTT as a major force shaping insect genome evolution.
horizontal transfer transposable elements insects genome evolution biogeography
Footnotes
1To whom correspondence may be addressed. Email: clement.gilbert30@gmail.com or jean.peccoud@univ-poitiers.fr.
Author contributions: J.P., R.C., and C.G. designed research; J.P., V.L., and C.G. performed research; J.P. and V.L. analyzed data; and J.P., R.C., and C.G. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1621178114/-/DCSupplemental.
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