skip to main content
US FlagAn official website of the United States government
dot gov icon
Official websites use .gov
A .gov website belongs to an official government organization in the United States.
https lock icon
Secure .gov websites use HTTPS
A lock ( lock ) or https:// means you've safely connected to the .gov website. Share sensitive information only on official, secure websites.


Title: The Presence of Ancient Core Genes Reveals Endogenization from Diverse Viral Ancestors in Parasitoid Wasps
Abstract The Ichneumonoidea (Ichneumonidae and Braconidae) is an incredibly diverse superfamily of parasitoid wasps that includes species that produce virus-like entities in their reproductive tracts to promote successful parasitism of host insects. Research on these entities has traditionally focused upon two viral genera Bracovirus (in Braconidae) and Ichnovirus (in Ichneumonidae). These viruses are produced using genes known collectively as endogenous viral elements (EVEs) that represent historical, now heritable viral integration events in wasp genomes. Here, new genome sequence assemblies for 11 species and 6 publicly available genomes from the Ichneumonoidea were screened with the goal of identifying novel EVEs and characterizing the breadth of species in lineages with known EVEs. Exhaustive similarity searches combined with the identification of ancient core genes revealed sequences from both known and novel EVEs. One species harbored a novel, independently derived EVE related to a divergent large double-stranded DNA (dsDNA) virus that manipulates behavior in other hymenopteran species. Although bracovirus or ichnovirus EVEs were identified as expected in three species, the absence of ichnoviruses in several species suggests that they are independently derived and present in two younger, less widespread lineages than previously thought. Overall, this study presents a novel bioinformatic approach for EVE discovery in genomes and shows that three divergent virus families (nudiviruses, the ancestors of ichnoviruses, and Leptopilina boulardi Filamentous Virus-like viruses) are recurrently acquired as EVEs in parasitoid wasps. Virus acquisition in the parasitoid wasps is a common process that has occurred in many more than two lineages from a diverse range of arthropod-infecting dsDNA viruses.  more » « less
Award ID(s):
1916914 1916788 1542290
PAR ID:
10291134
Author(s) / Creator(s):
; ;
Editor(s):
Wayne, Marta
Date Published:
Journal Name:
Genome Biology and Evolution
Volume:
13
Issue:
7
ISSN:
1759-6653
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Roossinck, Marilyn J. (Ed.)
    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. 
    more » « less
  2. ABSTRACT For insects known as parasitoid wasps, successful development as a parasite results in the death of the host insect. As a result of this lethal interaction, wasps and their hosts have coevolved strategies to gain an advantage in this evolutionary arms race. Although normally considered to be strict pathogens, some viruses have established persistent infections within parasitoid wasp lineages and are beneficial to wasps during parasitism. Heritable associations between viruses and parasitoid wasps have evolved independently multiple times, but most of these systems remain largely understudied with respect to viral origin, transmission and replication strategies of the virus, and interactions between the virus and host insects. Here, we report a detailed characterization of Diachasmimorpha longicaudata entomopoxvirus (DlEPV), a poxvirus found within the venom gland of Diachasmimorpha longicaudata wasps. Our results show that DlEPV exhibits similar but distinct transmission and replication dynamics compared to those of other parasitoid viral elements, including vertical transmission of the virus within wasps, as well as virus replication in both female wasps and fruit fly hosts. Functional assays demonstrate that DlEPV is highly virulent within fly hosts, and wasps without DlEPV have severely reduced parasitism success compared to those with a typical viral load. Taken together, the data presented in this study illustrate a novel case of beneficial virus evolution, in which a virus of unique origin has undergone convergent evolution with other viral elements associated with parasitoid wasps to provide an analogous function throughout parasitism. IMPORTANCE Viruses are generally considered to be disease-causing agents, but several instances of beneficial viral elements have been identified in insects called parasitoid wasps. These virus-derived entities are passed on through wasp generations and enhance the success of the wasps’ parasitic life cycle. Many parasitoid-virus partnerships studied to date exhibit common features among independent cases of this phenomenon, including a mother-to-offspring route of virus transmission, a restricted time and location for virus replication, and a positive effect of virus activity on wasp survival. Our characterization of Diachasmimorpha longicaudata entomopoxvirus (DlEPV), a poxvirus found in Diachasmimorpha longicaudata parasitoid wasps, represents a novel example of beneficial virus evolution. Here, we show that DlEPV exhibits functional similarities to known parasitoid viral elements that support its comparable role during parasitism. Our results also demonstrate unique differences that suggest DlEPV is more autonomous than other long-term viral associations described in parasitoid wasps. 
    more » « less
  3. Parrish, Colin R. (Ed.)
    ABSTRACT Bracoviruses (BVs) are endogenized nudiviruses in parasitoid wasps of the microgastroid complex (family Braconidae). Microgastroid wasps have coopted nudivirus genes to produce replication-defective virions that females use to transfer virulence genes to parasitized hosts. The microgastroid complex further consists of six subfamilies and ∼50,000 species but current understanding of BV gene inventories and organization primarily derives from analysis of two wasp species in the subfamily Microgastrinae ( Microplitis demolitor and Cotesia congregata ) that produce M. demolitor BV (MdBV) and C. congregata BV (CcBV). Notably, several genomic features of MdBV and CcBV remain conserved since divergence of M. demolitor and C. congregata ∼53 million years ago (MYA). However, it is unknown whether these conserved traits more broadly reflect BV evolution, because no complete genomes exist for any microgastroid wasps outside the Microgastrinae. In this regard, the subfamily Cheloninae is of greatest interest because it diverged earliest from the Microgastrinae (∼85 MYA) after endogenization of the nudivirus ancestor. Here, we present the complete genome of Chelonus insularis , which is an egg-larval parasitoid in the Cheloninae that produces C. insularis BV (CinsBV). We report that the inventory of nudivirus genes in C. insularis is conserved but are dissimilarly organized compared to M. demolitor and C. congregata . Reciprocally, CinsBV proviral segments share organizational features with MdBV and CcBV but virulence gene inventories exhibit almost no overlap. Altogether, our results point to the functional importance of a conserved inventory of nudivirus genes and a dynamic set of virulence genes for the successful parasitism of hosts. Our results also suggest organizational features previously identified in MdBV and CcBV are likely not essential for BV virion formation. IMPORTANCE Bracoviruses are a remarkable example of virus endogenization, because large sets of genes from a nudivirus ancestor continue to produce virions that thousands of wasp species rely upon to parasitize hosts. Understanding how these genes interact and have been coopted by wasps for novel functions is of broad interest in the study of virus evolution. This work characterizes bracovirus genome components in the parasitoid wasp Chelonus insularis , which together with existing wasp genomes captures a large portion of the diversity among wasp species that produce bracoviruses. Results provide new information about how bracovirus genome components are organized in different wasps while also providing additional insights on key features required for function. 
    more » « less
  4. Heritable symbionts display a wide variety of transmission strategies to travel from one insect generation to the next. Parasitoid wasps, one of the most diverse insect groups, maintain several heritable associations with viruses that are beneficial for wasp survival during their development as parasites of other insects. Most of these beneficial viral entities are strictly transmitted through the wasp germline as endogenous viral elements within wasp genomes. However, a beneficial poxvirus inherited by Diachasmimorpha longicaudata wasps, known as Diachasmimorpha longicaudata entomopoxvirus (DlEPV), is not integrated into the wasp genome and therefore may employ different tactics to infect future wasp generations. Here, we demonstrated that transmission of DlEPV is primarily dependent on parasitoid wasps, since viral transmission within fruit fly hosts of the wasps was limited to injection of the virus directly into the larval fly body cavity. Additionally, we uncovered a previously undocumented form of posthatch transmission for a mutualistic virus that entails external acquisition and localization of the virus within the adult wasp venom gland. We showed that this route is extremely effective for vertical and horizontal transmission of the virus within D. longicaudata wasps. Furthermore, the beneficial phenotype provided by DlEPV during parasitism was also transmitted with perfect efficiency, indicating an effective mode of symbiont spread to the advantage of infected wasps. These results provide insight into the transmission of beneficial viruses among insects and indicate that viruses can share features with cellular microbes during their evolutionary transitions into symbionts. 
    more » « less
  5. Abstract BackgroundInsects are an important reservoir of viral biodiversity, but the vast majority of viruses associated with insects have not been discovered. Recent studies have employed high-throughput RNA sequencing, which has led to rapid advances in our understanding of insect viral diversity. However, insect genomes frequently contain transcribed endogenous viral elements (EVEs) with significant homology to exogenous viruses, complicating the use of RNAseq for viral discovery. MethodsIn this study, we used a multi-pronged sequencing approach to study the virome of an important agricultural pest and prolific vector of plant pathogens, the potato aphidMacrosiphum euphorbiae. We first used rRNA-depleted RNAseq to characterize the microbes found in individual insects. We then used PCR screening to measure the frequency of two heritable viruses in a local aphid population. Lastly, we generated a quality draft genome assembly forM. euphorbiaeusing Illumina-corrected Nanopore sequencing to identify transcriptionally active EVEs in the host genome. ResultsWe found reads from two insect-specific viruses (aFlavivirusand anAmbidensovirus) in our RNAseq data, as well as a parasitoid virus (Bracovirus), a plant pathogenic virus (Tombusvirus), and two phages (Acinetobacter and APSE). However, our genome assembly showed that part of the ‘virome’ of this insect can be attributed to EVEs in the host genome. ConclusionOur work shows that EVEs have led to the misidentification of aphid viruses from RNAseq data, and we argue that this is a widespread challenge for the study of viral diversity in insects. 
    more » « less