Impact of Lateral Transfers on the Genomes of Lepidoptera

Abstract

Transfer of DNA sequences between species regardless of their evolutionary distance is very common in bacteria, but evidence that horizontal gene transfer (HGT) also occurs in multicellular organisms has been accumulating in the past few years. The actual extent of this phenomenon is underestimated due to frequent sequence filtering of “alien” DNA before genome assembly. However, recent studies based on genome sequencing have revealed, and experimentally verified, the presence of foreign DNA sequences in the genetic material of several species of Lepidoptera. Large DNA viruses, such as baculoviruses and the symbiotic viruses of parasitic wasps (bracoviruses), have the potential to mediate these transfers in Lepidoptera. In particular, using ultra-deep sequencing, newly integrated transposons have been identified within baculovirus genomes. Bacterial genes have also been acquired by genomes of Lepidoptera, as in other insects and nematodes. In addition, insertions of bracovirus sequences were present in the genomes of certain moth and butterfly lineages, that were likely corresponding to rearrangements of ancient integrations. The viral genes present in these sequences, sometimes of hymenopteran origin, have been co-opted by lepidopteran species to confer some protection against pathogens.

Cotesia congregata Bracovirus Circles Encoding PTP and Ankyrin Genes Integrate into the DNA of Parasitized Manduca sexta Hemocytes

“…Unraveling the mechanisms and extent of PDV integration events (i.e., investigating integration of other circles and integration in other tissues, including germinal cells) will not only allow us to better understand virulence strategies developed by parasitoid wasps to successfully parasitize their lepidopteran hosts but might also provide the mechanism of recently uncovered horizontal gene transfer between parasitic wasps, PDVs, and the genomes of moths and butterflies. Indeed, in some cases CcBV DNA containing genes of wasp origin have been found to be present in the genomes of many lepidopteran species, including the iconic Monarch species (61)(62)(63). However, unlike BV sequences identified in C. sesamiae wasps, we could not find a complete circle inserted in the genome of Lepidoptera, which could be due to the fact that the insertions are ancient and have undertaken many rearrangements after circle integration.…”

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

“…Following a number of reports of TE insertions in baculoviruses [38–42], recent surveys based on deep sequencing of viral genomes have revealed an abundant presence of host TEs, some of which match documented cases of HTT [11,12]. Based on these findings, the high potential of baculoviruses as vectors of HTT in Lepidoptera has been previously emphasized [3]. Some authors have even explicitly suggested that considering the high prevalence of baculoviruses in Lepidoptera, an elevated HTT rate in that clade would provide support for their implication [20] (page 271).…”

Co‐option of microbial associates by insects and their impact on plant–folivore interactions

“…Some HGTs have provided new functionality and enabled the recipients to acquire traits that facilitate nutrition, protect against adverse environments, contend with toxic diets, and, for our purposes here, adapt to host plants in the case of herbivores (Husnik & McCutcheon, ). The co‐opting of microbial genes from bacteria, baculoviruses, polydnaviruses (PDVs; especially bracoviruses), and fungi has shaped the genomes of many herbivorous insects: Lepidoptera (Drezen, Josse, et al, ), Coleoptera (Kirsch et al, ), and others (Wybouw, Van Leeuwen, & Dermauw, ). Such HGT events have enabled herbivore speciation and the successful colonization of host plants.…”