Global survey of mobile DNA horizontal transfer in arthropods reveals Lepidoptera as a prime hotspot.

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. Author summary Transposable elements are chunks of DNA that can produce copies of themselves. New copies usually insert in the genome of their carrier but are occasionally subject to horizontal transmission between organisms, sometimes belonging to evolutionarily-distant lineages. Previous surveys have established that the probability of such events is largely conditioned by the transposition mechanism. For example, elements with an RNA intermediate tend to be less frequently involved in horizontal transfers. Here we investigate host taxa as another potential explanatory factor of variation in horizontal transfer rates. 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. Previous studies have established that Lepidoptera are also commonly attacked by baculoviruses, large viruses that can transport host DNA. Taken together, these findings point to baculoviruses as a major suspect for transposable elements transfers across arthropod species.