Cited by 5Chromosomal and Genetic VariationsGenomics and Phylogenetic StudiesEvolution and Genetic Dynamics

The DOI matches its Crossref record; 5 of the 5 references it cites were found in a registry or an index.

Discovery of novel non-retroviral endogenous viral elements reveals their long-term integration history in spiders

Open access
Hu, Hengrui, Vlak, Just M., Hu, Zhihong, Wang, Manli·2025·Nature Communications

Published version of a preprint

Abstract

Abstract Endogenous viral elements (EVEs) are widespread in the genomes of various organisms and have played a crucial role in evolution. Historically, research on EVEs primarily focused on those derived from retroviruses; however, the significance of non-retroviral EVEs (nrEVEs) has gradually gained recognition. In this study, we employed a novel approach that combines protein structure prediction with sequence analysis to identify a large group of previously unrecognized nrEVEs across spider genomes. Additionally, we identified nrEVE-related messenger RNAs, microRNAs, and PIWI-interacting RNAs in spiders, suggesting that these nrEVEs may be functionally active. We also experimentally confirmed the presence of spider nrEVEs and their transcripts in individual spiders. Evolutionary analysis suggests that these spider nrEVEs originated from an ancestral nuclear arthropod large DNA virus (NALDV) belonging to the order Lefavirales, class Naldaviricetes, approximately 270 million years ago. The integration of these nrEVEs occurred prior to the last common ancestor of the Araneae, indicating a long-term co-evolutionary relationship between these nrEVEs and spiders. Our findings reveal a novel group of nrEVEs and provide valuable insights into their evolutionary relationship with arthropods.

Overview

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1038/s41467-025-61035-2

Cites

5 of 5 references verified0 citation errors · 0 not checkable

Statistics

Verification

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Citations

Cites

Flagged first, then by citations

Research works printed but not linked: 57

  1. Feschotte, C. & Gilbert, C. Endogenous viruses: insights into viral evolution and impact on host biology. Nat. Rev. Genet. 13, 283–296 (2012). · DOI
  2. Holmes, E. C. The evolution of endogenous viral elements. Cell Host Microbe 10, 368–377 (2011). · DOI
  3. Weiss, R. A. The discovery of endogenous retroviruses. Retrovirology 3, 67 (2006). · DOI
  4. Horie, M. et al. Endogenous non-retroviral RNA virus elements in mammalian genomes. Nature 463, 84–87 (2010). · DOI
  5. Houe, V., Bonizzoni, M. & Failloux, A. B. Endogenous non-retroviral elements in genomes of Aedes mosquitoes and vector competence. Emerg. Microbes Infect. 8, 542–555 (2019). · DOI
  6. Huang, H.-J. et al. Co-option of a non-retroviral endogenous viral element in planthoppers. Nat. Commun. 14 https://doi.org/10.1038/s41467-023-43186-2 (2023). · DOI
  7. Frank, J. A. & Feschotte, C. Co-option of endogenous viral sequences for host cell function. Curr. Opin. Virol. 25, 81–89 (2017). · DOI
  8. Aiewsakun, P. & Katzourakis, A. Endogenous viruses: connecting recent and ancient viral evolution. Virology 479-480, 26–37 (2015). · DOI
  9. Johnson, W. E. Origins and evolutionary consequences of ancient endogenous retroviruses. Nat. Rev. Microbiol. 17, 355–370 (2019). · DOI
  10. Regier, J. C. et al. Arthropod relationships revealed by phylogenomic analysis of nuclear protein-coding sequences. Nature 463, 1079–1083 (2010). · DOI
  11. van Oers, M. M. et al. Developments in the classification and nomenclature of arthropod-infecting large DNA viruses that contain pif genes. Arch. Virol. 168, 182 (2023). · DOI
  12. Koonin, E. V. et al. Global organization and proposed megataxonomy of the virus world. Microbiol. Mol. Biol. R. 84, e00061–19 (2020). · DOI
  13. Passarelli, A. L. & Guarino, L. A. Baculovirus late and very late gene regulation. Curr. Drug Targets 8, 1103–1115 (2007). · DOI
  14. Lin, C. L. et al. Persistent Hz-1 virus infection in insect cells: evidence for insertion of viral DNA into host chromosomes and viral infection in a latent status. J. Virol. 73, 128–139 (1999). · DOI
  15. Cheng, R. L., Li, X. F. & Zhang, C. X. Nudivirus remnants in the genomes of arthropods. Genome Biol. Evol. 12, 578–588 (2020). · DOI
  16. Bezier, A. et al. Polydnaviruses of braconid wasps derive from an ancestral nudivirus. Science 323, 926–930 (2009). · DOI
  17. Strand, M. R. & Burke, G. R. Polydnaviruses: evolution and function. Curr. Issues Mol. Biol. 34, 163–181 (2019).
  18. Kawato, S. et al. Crustacean genome exploration reveals the evolutionary origin of white spot syndrome virus. J. Virol. 93 https://doi.org/10.1128/JVI.01144-18 (2019). · DOI
  19. Guinet, B. et al. Endoparasitoid lifestyle promotes endogenization and domestication of dsDNA viruses. Elife 12 https://doi.org/10.7554/eLife.85993 (2023). · DOI
  20. Legg, D. A., Sutton, M. D. & Edgecombe, G. D. Arthropod fossil data increase congruence of morphological and molecular phylogenies. Nat. Commun. 4, 2485 (2013). · DOI
  21. Kulkarni, S., Wood, H. M. & Hormiga, G. Advances in the reconstruction of the spider tree of life: a roadmap for spider systematics and comparative studies. Cladistics 39, 479–532 (2023). · DOI
  22. Sanggaard, K. W. et al. Spider genomes provide insight into composition and evolution of venom and silk. Nat. Commun. 5, 3765 (2014). · DOI
  23. Mihara, T. et al. Linking virus genomes with host taxonomy. Viruses 8, 66 (2016). · DOI
  24. Liu, S., Coates, B. S. & Bonning, B. C. Endogenous viral elements integrated into the genome of the soybean aphid, Aphis glycines. Insect Biochem. Mol. Biol. 123, 103405 (2020). · DOI
  25. Burke, G. R., Simmonds, T. J., Sharanowski, B. J. & Geib, S. M. Rapid viral symbiogenesis via changes in parasitoid wasp genome architecture. Mol. Biol. Evol. 35, 2463–2474 (2018). · DOI
  26. Pichon, A. et al. Recurrent DNA virus domestication leading to different parasite virulence strategies. Sci. Adv. 1, e1501150 (2015). · DOI
  27. Nayfach, S. et al. CheckV assesses the quality and completeness of metagenome-assembled viral genomes. Nat. Biotechnol. 39, 578–585 (2021). · DOI
  28. Hackl, T., Duponchel, S., Barenhoff, K., Weinmann, A. & Fischer, M. G. Virophages and retrotransposons colonize the genomes of a heterotrophic flagellate. Elife 10, e72674 (2021). · DOI
  29. Guinet, B. et al. A novel and diverse family of filamentous DNA viruses associated with parasitic wasps. Virus Evol. 10, veae022 (2024). · DOI
  30. Ter Horst, A. M., Nigg, J. C., Dekker, F. M. & Falk, B. W. Endogenous viral elements are widespread in arthropod genomes and commonly give rise to PIWI-interacting RNAs. J. Virol. 93. https://doi.org/10.1128/JVI.02124-18 (2019) · DOI
  31. Thézé, J., Bézier, A., Periquet, G., Drezen, J.-M. & Herniou, E. A. Paleozoic origin of insect large dsDNA viruses. Proc. Natl. Acad. Sci. USA 108, 15931–15935 (2011). · DOI
  32. Murphy, N., Banks, J. C., Whitfield, J. B. & Austin, A. D. Phylogeny of the parasitic microgastroid subfamilies (Hymenoptera: Braconidae) based on sequence data from seven genes, with an improved time estimate of the origin of the lineage. Mol. Phylogenet. Evol. 47, 378–395 (2008). · DOI
  33. Selden, P. A., Anderson, H. M. & Anderson, J. M. A review of the fossil record of spiders (Araneae) with special reference to Africa, and description of a new specimen from the Triassic Molteno Formation of South Africa. Afr. Invertebrates 50 1, 105 (2009. · DOI
  34. Selden, P. A. Fossil mesothele spiders. Nature 379, 498–499 (1996). · DOI
  35. Selden, P. A., Shear, W. A. & Bonamo, P. M. A spider and other arachnids from the Devonian of New York, and reinterpretations of Devonian Araneae. Palaeontology 34, 241–281 (1991).
  36. Bond, J. E. et al. Phylogenomics resolves a spider backbone phylogeny and rejects a prevailing paradigm for orb web evolution. Curr. Biol. 24, 1765–1771 (2014). · DOI
  37. Wallau, G. L. RNA virus EVEs in insect genomes. Curr. Opin. Insect Sci. 49, 42–47 (2022). · DOI
  38. Frank, J. A. et al. Evolution and antiviral activity of a human protein of retroviral origin. Science 378, 422–428 (2022). · DOI
  39. Gilbert, C. & Belliardo, C. The diversity of endogenous viral elements in insects. Curr. Opin. Insect Sci. 49, 48–55 (2022). · DOI
  40. Kumar, S. et al. TimeTree 5: an expanded resource for species divergence times. Mol. Biol. Evol. 39, msac174 (2022). · DOI
  41. Gilbert, C. & Cordaux, R. Viruses as vectors of horizontal transfer of genetic material in eukaryotes. Curr. Opin. Virol. 25, 16–22 (2017). · DOI
  42. Jia, X. et al. Architecture of the baculovirus nucleocapsid revealed by cryo-EM. Nat. Commun. 14, 7481 (2023). · DOI
  43. Nomburg, J. et al. Birth of protein folds and functions in the virome. Nature 633, 710–717 (2024). · DOI
  44. Kieft, K., Adams, A., Salamzade, R., Kalan, L. & Anantharaman, K. vRhyme enables binning of viral genomes from metagenomes. Nucleic Acids Res. 50, e83 (2022). · DOI
  45. Mirdita, M. et al. ColabFold: making protein folding accessible to all. Nat. Methods 19, 679–682 (2022). · DOI · Paper page
  46. Singh, U. & Wurtele, E. S. orfipy: a fast and flexible tool for extracting ORFs. Bioinformatics 37, 3019–3020 (2021). · DOI
  47. Shannon, P. et al. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 13, 2498–2504 (2003). · DOI · Paper page
  48. Gabler, F. et al. Protein sequence analysis using the MPI bioinformatics toolkit. Curr. Protoc. Bioinforma. 72, e108 (2020). · DOI · Paper page
  49. Steinegger, M. & Soding, J. MMseqs2 enables sensitive protein sequence searching for the analysis of massive data sets. Nat. Biotechnol. 35, 1026–1028 (2017). · DOI · Paper page
  50. Katoh, K., Misawa, K., Kuma, K. & Miyata, T. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 30, 3059–3066 (2002). · DOI · Paper page
  51. Capella-Gutierrez, S., Silla-Martinez, J. M. & Gabaldon, T. trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25, 1972–1973 (2009). · DOI
  52. Minh, B. Q. et al. IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Mol. Biol. Evol. 37, 1530–1534 (2020). · DOI · Paper page
  53. Suchard, M. A. et al. Bayesian phylogenetic and phylodynamic data integration using BEAST 1.10. Virus Evol. 4, vey016 (2018). · DOI
  54. Langmead, B. & Salzberg, S. L. Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357–359 (2012). · DOI · Paper page
  55. Danecek, P. et al. Twelve years of SAMtools and BCFtools. Gigascience 10 https://doi.org/10.1093/gigascience/giab008 (2021). · DOI
  56. Grubaugh, N. D. et al. An amplicon-based sequencing framework for accurately measuring intrahost virus diversity using PrimalSeq and iVar. Genome Biol. 20, 8 (2019). · DOI
  57. Chen, C. et al. TBtools-II: a “one for all, all for one” bioinformatics platform for biological big-data mining. Mol. Plant 16, 1733–1742 (2023). · DOI

Metadata

Authors
Hu, H., Vlak, J. M., Hu, Z., & Wang, M.
Affiliations
  • Chinese Academy of Sciences (CN)
  • Wageningen University & Research (NL)
Corresponding author
Wang, Manli
Venue
Nature Communications
Published
2025-07-01
Volume
16
Issue
1
Pages
6006-6006
ISSN
2041-1723 (ISSN-L)
OpenAlex
W4411847105
Cited by
5
References
5
Citations by year
2026: 4 · 2025: 1
FWCI
2.70
Type
journal article
Language
en
Open access
Locations
  • Nature Communications (publishedVersion, cc-by-nc-nd)
  • Research Square (acceptedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by-nc-nd)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Socio-Environmental Systems Modeling (submittedVersion, cc-by-nc-nd)
Funders
National Natural Science Foundation of China (32370182, 37277104, 32170156)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Chromosomal and Genetic Variations
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
Keywords
endogenous viral elements, spiders, siRNA, piRNA, arthropod evolution, genome evolution
MeSH terms
Animals, DNA Viruses, Phylogeny, Spiders, Virus Integration, Evolution, Molecular, RNA, Small Interfering

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review