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

PLoS Genet. 2019 Feb 1;15(2):e1007965. doi: 10.1371/journal.pgen.1007965. eCollection 2019 Feb.

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.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Arthropods / classification
  • Arthropods / genetics*
  • Baculoviridae / genetics
  • DNA Transposable Elements*
  • Evolution, Molecular
  • Gene Transfer, Horizontal
  • Genetic Variation
  • Genome, Insect
  • Lepidoptera / classification
  • Lepidoptera / genetics*
  • Lepidoptera / virology
  • Models, Genetic
  • Phylogeny
  • Polynesia

Substances

  • DNA Transposable Elements

Grants and funding

This work was supported by the Centre National de la Recherche Scientifique (CNRS) (ATIP grant SymbioCode to S.C.), the Agence Nationale de la Recherche (Horizon grant to S.C.: ANR-17-CE02-0021-02). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.