title: Recurrent Domestication by Lepidoptera of Genes from Their Parasites Mediated by Bracoviruses.
abstract: Bracoviruses are symbiotic viruses associated with tens of thousands of species of parasitic wasps that develop within the body of lepidopteran hosts and that collectively parasitize caterpillars of virtually every lepidopteran species. Viral particles are produced in the wasp ovaries and injected into host larvae with the wasp eggs. Once in the host body, the viral DNA circles enclosed in the particles integrate into lepidopteran host cell DNA. Here we show that bracovirus DNA sequences have been inserted repeatedly into lepidopteran genomes, indicating this viral DNA can also enter germline cells. The original mode of Horizontal Gene Transfer (HGT) unveiled here is based on the integrative properties of an endogenous virus that has evolved as a gene transfer agent within parasitic wasp genomes for ≈100 million years. Among the bracovirus genes thus transferred, a phylogenetic analysis indicated that those encoding C-type-lectins most likely originated from the wasp gene set, showing that a bracovirus-mediated gene flux exists between the 2 insect orders Hymenoptera and Lepidoptera. Furthermore, the acquisition of bracovirus sequences that can be expressed by Lepidoptera has resulted in the domestication of several genes that could result in adaptive advantages for the host. Indeed, functional analyses suggest that two of the acquired genes could have a protective role against a common pathogen in the field, baculovirus. From these results, we hypothesize that bracovirus-mediated HGT has played an important role in the evolutionary arms race between Lepidoptera and their pathogens.
authors.affiliation: Department of Genetics, Universitat de València, Burjassot, Spain; Estructura de Recerca Interdisciplinar en Biotecnologia i Biomedicina (ERI BIOTECMED), Universitat de València, Burjassot, Spain.
authors.forename: Laila
authors.initials: L
authors.lastname: Gasmi
authors.affiliation: Institut de Recherche sur la Biologie de l'Insecte, UMR CNRS 7261, UFR des Sciences et Techniques, Université François Rabelais, Tours, France.
authors.forename: Helene
authors.initials: H
authors.lastname: Boulain
authors.affiliation: Institut de Recherche sur la Biologie de l'Insecte, UMR CNRS 7261, UFR des Sciences et Techniques, Université François Rabelais, Tours, France.
authors.forename: Jeremy
authors.initials: J
authors.lastname: Gauthier
authors.affiliation: Laboratoire Evolution, Génomes, Comportement, Ecologie, CNRS/Université Paris-Sud UMR9191, IRD UMR247, Université Paris-Saclay, Gif-sur-Yvette, France.
authors.forename: Aurelie
authors.initials: A
authors.lastname: Hua-Van
authors.affiliation: Institut de Recherche sur la Biologie de l'Insecte, UMR CNRS 7261, UFR des Sciences et Techniques, Université François Rabelais, Tours, France.
authors.forename: Karine
authors.initials: K
authors.lastname: Musset
authors.affiliation: Department of Genetics, Universitat de València, Burjassot, Spain; Estructura de Recerca Interdisciplinar en Biotecnologia i Biomedicina (ERI BIOTECMED), Universitat de València, Burjassot, Spain.
authors.forename: Agata K
authors.initials: AK
authors.lastname: Jakubowska
authors.affiliation: Commissariat à l'Energie Atomique et aux Energies Alternatives, Genoscope (Centre National de Séquençage), Evry, France.
authors.forename: Jean-Marc
authors.initials: JM
authors.lastname: Aury
authors.affiliation: Diversity, Genomes and Interactions Between Microorganisms and Insects Laboratory, INRA (UMR 1333), Université de Montpellier, Place Eugène Bataillon, CC 101, Montpellier, France.
authors.forename: Anne-Nathalie
authors.initials: AN
authors.lastname: Volkoff
authors.affiliation: Institut de Recherche sur la Biologie de l'Insecte, UMR CNRS 7261, UFR des Sciences et Techniques, Université François Rabelais, Tours, France.
authors.forename: Elisabeth
authors.initials: E
authors.lastname: Huguet
authors.affiliation: Department of Genetics, Universitat de València, Burjassot, Spain; Estructura de Recerca Interdisciplinar en Biotecnologia i Biomedicina (ERI BIOTECMED), Universitat de València, Burjassot, Spain.
authors.forename: Salvador
authors.initials: S
authors.lastname: Herrero
authors.affiliation: Institut de Recherche sur la Biologie de l'Insecte, UMR CNRS 7261, UFR des Sciences et Techniques, Université François Rabelais, Tours, France.
authors.forename: Jean-Michel
authors.initials: JM
authors.lastname: Drezen
mesh_terms: D000818:Animals; D001483:Base Sequence; D004279:DNA, Viral; D017344:Genes, Insect; D007915:Lepidoptera / Q000469:parasitology*; D008969:Molecular Sequence Data; D018071:Polydnaviridae / Q000235:genetics / Q000502:physiology*; D018411:Spodoptera / Q000235:genetics; D014863:Wasps / Q000235:genetics*
chemical_list: D004279:DNA, Viral