Massive horizontal transfer of transposable elements in insects

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 H orizontal transfer (HT) is the transmission of genetic material between organisms through a mechanism other than reproduction. In prokaryotes, HT is pervasive, its mechanisms are well understood, and it is now viewed as one of the main forces shaping genome architecture and evolution (1, 2). In contrast, the study of HT in eukaryotes is less documented, but has been increasingly investigated. The majority of genes horizontally acquired by eukaryotes come from bacteria, but the extent to which these transfers have contributed to eukaryote evolution is still unclear (3, 4). Gene transfers from eukaryote to eukaryote appear to be largely limited to filamentous organisms, such as oomycetes and fungi (5, 6).In animals and plants, very few cases of such horizontal gene transfers (HGTs) have been reported so far (7,8). In fact, most of the genetic material that is horizontally transferred in animals and plants consists of transposable elements (TEs) (9-11), which are pieces of DNA able to move from a chromosomal locus to another (12). The greater ability of TEs to move between organisms certainly relates to their intrinsic ability to transpose within genomes, which genes cannot do. HT of TEs (HTT) may allow these elements to enter naive genomes, which they invade by making copies of themselves, and then escape before they become fully silenced by anti-TE defenses (13). A growing number of studies have identified such HTT (11,[14][15][16]. However, a common drawback of these studies has been the inclusion of a limited set of TEs (11) or organisms (16), which hampers our understanding of the breadth of HTT, its contribution to genome evolution, and of the factors and barriers shaping these transfe...

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“…With this aim in mind, we recently conducted a systematic analysis of HTT among all 195 insect species whose genome sequences were publicly available . Our analysis showed that at least 2248 HTT events occurred among these insects in the last 10 million years.…”

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