Abstract
Insects are known to host a wide variety of beneficial microbes that are fundamental to many aspects of their biology and have substantially shaped their evolution. Notably, parasitoid wasps have repeatedly evolved beneficial associations with viruses that enable developing wasps to survive as parasites that feed from other insects. Ongoing genomic sequencing efforts have revealed that most of these virus-derived entities are fully integrated into the genomes of parasitoid wasp lineages, representing endogenous viral elements (EVEs) that retain the ability to produce virus or virus-like particles within wasp reproductive tissues. All documented parasitoid EVEs have undergone similar genomic rearrangements compared to their viral ancestors characterized by viral genes scattered across wasp genomes and specific viral gene losses. The recurrent presence of viral endogenization and genomic reorganization in beneficial virus systems identified to date suggest that these features are crucial to forming heritable alliances between parasitoid wasps and viruses. Here, our genomic characterization of a mutualistic poxvirus associated with the wasp Diachasmimorpha longicaudata, known as Diachasmimorpha longicaudata entomopoxvirus (DlEPV), has uncovered the first instance of beneficial virus evolution that does not conform to the genomic architecture shared by parasitoid EVEs with which it displays evolutionary convergence. Rather, DlEPV retains the exogenous viral genome of its poxvirus ancestor and the majority of conserved poxvirus core genes. Additional comparative analyses indicate that DlEPV is related to a fly pathogen and contains a novel gene expansion that may be adaptive to its symbiotic role. Finally, differential expression analysis during virus replication in wasps and fly hosts demonstrates a unique mechanism of functional partitioning that allows DlEPV to persist within and provide benefit to its parasitoid wasp host.
Highlights
Microbial symbionts have been increasingly identified as major drivers of animal evolution due to the novel capabilities microbes provide to their hosts and the speed at which symbiosis can cause adaptive change in animal lineages [1,2]
Given the importance of viral genome integration in the overall stability of parasitoid wasp-endogenous viral elements (EVEs) systems, we identified a novel strategy used by Diachasmimorpha longicaudata entomopoxvirus (DlEPV) to maintain its relationship with D. longicaudata despite its lack of endogenization
The study of poxviruses has historically focused on CPVs and the prototype CPV, known as vaccinia virus (VACV), due to the societal impact of smallpox [36]
Summary
Microbial symbionts have been increasingly identified as major drivers of animal evolution due to the novel capabilities microbes provide to their hosts and the speed at which symbiosis can cause adaptive change in animal lineages [1,2]. Parasitoid wasp lineages have repeatedly acquired heritable viruses in conjunction with evolutionary arms race dynamics between wasps and their hosts [10,11,12]. Many of these associations are extraordinary examples of endogenous viral elements (EVEs) within wasp genomes, in which components of viral machinery are retained from their pathogenic ancestors to produce virus or virus-like particles within wasp ovaries [13,14]. The resulting virus-derived particles accompany wasp eggs when delivered into host insects and can function to protect parasitoid eggs from attack by the host immune system and/or actively disrupt host developmental and immunological pathways [10,15,16]
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