The parasitoid wasp Venturia canescens is an important biological control agent of stored products moth pests and serves as a model to study the function and evolution of domesticated endogenous viruses (DEVs). The DEVs discovered in V. canescens are known as virus-like particles (VcVLPs), which are produced using nudivirus-derived components and incorporate wasp-derived virulence proteins instead of packaged nucleic acids. Previous studies of virus-derived components in the V. canescens genome identified 53 nudivirus-like genes organized in six gene clusters and several viral pseudogenes, but how VcVLP genes are organized among wasp chromosomes following their integration in the ancestral wasp genome is largely unknown. Here, we present a chromosomal scale genome of V. canescens consisting of 11 chromosomes and 56 unplaced small scaffolds. The genome size is 290.8 Mbp with a N50 scaffold size of 24.99 Mbp. A high-quality gene set including 11,831 protein-coding genes were produced using RNA-Seq data as well as publicly available peptide sequences from related Hymenoptera. A manual annotation of genes of viral origin produced 61 intact and 19 pseudogenized nudivirus-derived genes. The genome assembly revealed that two previously identified clusters were joined into a single cluster and a total of 5 gene clusters comprising of 60 intact nudivirus-derived genes were located in three chromosomes. In contrast, pseudogenes are dispersed among 8 chromosomes with only 4 pseudogenes associated with nudivirus gene clusters. The architecture of genes encoding VcVLP components suggests it originates from a recent virus acquisition and there is a link between the processes of dispersal and pseudogenization. This high-quality genome assembly and annotation represents the first chromosome-scale assembly for parasitoid wasps associated with VLPs, and is publicly available in the National Center for Biotechnology Information Genome and RefSeq databases, providing a valuable resource for future studies of DEVs in parasitoid wasps.
Genome of the Parasitoid Wasp Diachasma alloeum, an Emerging Model for Ecological Speciation and Transitions to Asexual Reproduction
Abstract Parasitoid wasps are among the most speciose animals, yet have relatively few available genomic resources. We report a draft genome assembly of the wasp Diachasma alloeum (Hymenoptera: Braconidae), a host-specific parasitoid of the apple maggot fly Rhagoletis pomonella (Diptera: Tephritidae), and a developing model for understanding how ecological speciation can “cascade” across trophic levels. Identification of gene content confirmed the overall quality of the draft genome, and we manually annotated ∼400 genes as part of this study, including those involved in oxidative phosphorylation, chemosensation, and reproduction. Through comparisons to model hymenopterans such as the European honeybee Apis mellifera and parasitoid wasp Nasonia vitripennis, as well as a more closely related braconid parasitoid Microplitis demolitor, we identified a proliferation of transposable elements in the genome, an expansion of chemosensory genes in parasitoid wasps, and the maintenance of several key genes with known roles in sexual reproduction and sex determination. The D. alloeum genome will provide a valuable resource for comparative genomics studies in Hymenoptera as well as specific investigations into the genomic changes associated with ecological speciation and transitions to asexuality.
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- Award ID(s):
- 1638997
- NSF-PAR ID:
- 10188268
- Date Published:
- Journal Name:
- Genome Biology and Evolution
- Volume:
- 11
- Issue:
- 10
- ISSN:
- 1759-6653
- Page Range / eLocation ID:
- 2767 to 2773
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract -
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
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null (Ed.)Abstract Background Parasitoidism, a specialized life strategy in which a parasite eventually kills its host, is frequently found within the insect order Hymenoptera (wasps, ants and bees). A parasitoid lifestyle is one of two dominant life strategies within the hymenopteran superfamily Cynipoidea, with the other being an unusual plant-feeding behavior known as galling. Less commonly, cynipoid wasps exhibit inquilinism, a strategy where some species have adapted to usurp other species’ galls instead of inducing their own. Using a phylogenomic data set of ultraconserved elements from nearly all lineages of Cynipoidea, we here generate a robust phylogenetic framework and timescale to understand cynipoid systematics and the evolution of these life histories. Results Our reconstructed evolutionary history for Cynipoidea differs considerably from previous hypotheses. Rooting our analyses with non-cynipoid outgroups, the Paraulacini, a group of inquilines, emerged as sister-group to the rest of Cynipoidea, rendering the gall wasp family Cynipidae paraphyletic. The families Ibaliidae and Liopteridae, long considered archaic and early-branching parasitoid lineages, were found nested well within the Cynipoidea as sister-group to the parasitoid Figitidae. Cynipoidea originated in the early Jurassic around 190 Ma. Either inquilinism or parasitoidism is suggested as the ancestral and dominant strategy throughout the early evolution of cynipoids, depending on whether a simple (three states: parasitoidism, inquilinism and galling) or more complex (seven states: parasitoidism, inquilinism and galling split by host use) model is employed. Conclusions Our study has significant impact on understanding cynipoid evolution and highlights the importance of adequate outgroup sampling. We discuss the evolutionary timescale of the superfamily in relation to their insect hosts and host plants, and outline how phytophagous galling behavior may have evolved from entomophagous, parasitoid cynipoids. Our study has established the framework for further physiological and comparative genomic work between gall-making, inquiline and parasitoid lineages, which could also have significant implications for the evolution of diverse life histories in other Hymenoptera.more » « less
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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
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Emerson, J J (Ed.)Abstract Dinocampus coccinellae (Hymenoptera: Braconidae) is a generalist parasitoid wasp that parasitizes >50 species of predatory lady beetles (Coleoptera: Coccinellidae), with thelytokous parthenogeny as its primary mode of reproduction. Here, we present the first high-quality genome of D. coccinellae using a combination of short- and long-read sequencing technologies, followed by assembly and scaffolding of chromosomal segments using Chicago + HiC technologies. We also present a first-pass ab initio and a reference-based genome annotation and resolve timings of divergence and evolution of (1) solitary behavior vs eusociality, (2) arrhenotokous vs thelytokous parthenogenesis, and (3) rates of gene loss and gain among Hymenopteran lineages. Our study finds (1) at least 2 independent origins of eusociality and solitary behavior among Hymenoptera, (2) 2 independent origins of thelytokous parthenogenesis from ancestral arrhenotoky, and (3) accelerated rates of gene duplications, loss, and gain along the lineages leading to D. coccinellae. Our work both affirms the ancient divergence of Braconid wasps from ancestral Hymenopterans and accelerated rates of evolution in response to adaptations to novel hosts, including polyDNA viral coevolution.more » « less
- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1093/gbe/evz205
