Domestication of bracoviruses for use as gene delivery vectors by Microplitis demolitor parasitoid wasps

Parasitoid wasps (order Hymenoptera) lay their eggs into other insects, where their progeny develop, feed, and ultimately kill their hosts. This creates an arms race between wasps and their hosts. Wasps in the subfamily Braconidae have evolved an unusual weapon in their parasitism arsenal: a symbiotic association with viruses in the genus Bracovirus (Polydnaviridae). Bracoviruses evolved from a pathogenic ancestor that was endogenized into wasp chromosomes approximately 100 million years ago. Bracovirus genomes are transmitted through Mendelian inheritance, and replication has become confined to specialized cells in the ovaries of associated wasps. Wasps inject virus particles into their hosts along with eggs and virulence genes encoded by the virus to prevent the host immune system from killing wasp progeny. Here we describe the genomic architecture of the virus, which is unique compared to all other viruses. Viral gene content is a compilation of ancestral virus genes and virulence genes co-opted from a variety of sources including the wasp genome itself. These two types of genes are separated in the wasp genome; virulence genes are part of DNA segments that will become circularized and packaged into virions, whereas ancestral virus replication genes are located elsewhere in the genome and are never delivered into hosts. This genomic organization has allowed wasps to domesticate bracoviruses into gene delivery vectors for parasitism of hosts. Parasitoid wasps and their hosts are the most species rich animals on earth. Our research describes an ancient viral association that has profoundly affected insect evolution.