Abstract

More than any other genome components, Transposable Elements (TEs) have the capacity to move across species barriers through Horizontal Transfer (HT), with substantial evolutionary consequences. Previous large-scale surveys, based on full-genomes comparisons, have revealed the transposition mode as an important predictor of HT rates variation across TE superfamilies. However, host biology could represent another major explanatory factor, one that needs to be investigated through extensive taxonomic sampling. Here we test this hypothesis using a field collection of 460 arthropod species from Tahiti and surrounding islands. Through targeted massive parallel sequencing, we uncover patterns of HT in three widely-distributed TE superfamilies with contrasted modes of transposition. In line with earlier findings, the DNA transposons under study (TC1-Mariner) were found to transfer horizontally at the highest frequency, closely followed by the LTR superfamily (Copia), in contrast with the non-LTR superfamily (Jockey), that mostly diversifies through vertical inheritance and persists longer within genomes. Strikingly, across all superfamilies, we observe a marked excess of HTs in Lepidoptera, an insect order that also commonly hosts baculoviruses, known for their ability to transport host TEs. These results turn the spotlight on baculoviruses as major potential vectors of TEs in arthropods, and further emphasize the importance of non-vertical TE inheritance in genome evolution.

Highlights

  • Metazoans are mostly sexual organisms, meaning that their reproduction is strictly associated with a process of massive genomic exchanges between two close relatives

  • Using targeted sequencing in hundreds of insects and other arthropod species collected in South Pacific islands, we found that butterflies and moths (Lepidoptera) show an abnormally elevated rate of horizontal transfers

  • In addition to revealing the abundance of horizontally-acquired DNA within genomes, this study confirmed the previously suggested trend that variation in HTT rates can in large part be explained by the transposable elements (TEs) biology: DNA transposons tend to move more often than LTR-retroelements, which move more often than non-LTR retroelements [6,9,10]

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Summary

Introduction

Metazoans are mostly sexual organisms, meaning that their reproduction is strictly associated with a process of massive genomic exchanges between two close relatives They occasionally acquire DNA from evolutionarily-distant lineages, which produces an important source of heritable variation and deeply affects genomes’ evolutionary dynamics [1,2,3,4,5]. We investigate the hypothesis that host taxa might represent an additional important predictor of HTT rates To this end, instead of using whole-genome databases, subject to strong inherent taxonomic biases, we use a large and random field sample of arthropods to uncover patterns of HTT in three widespread TE superfamilies. This design allows us to assess variation and commonalities in patterns of HTT across TE superfamilies and across host taxa, based on species that co-occur in a geographically-delimited region

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