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Evolutionary origins of the SARS-CoV-2 sarbecovirus lineage responsible for the COVID-19 pandemic
Open accessPublished version of a preprint
Abstract
There are outstanding evolutionary questions on the recent emergence of human coronavirus SARS-CoV-2 including the role of reservoir species, the role of recombination and its time of divergence from animal viruses. We find that the sarbecoviruses-the viral subgenus containing SARS-CoV and SARS-CoV-2-undergo frequent recombination and exhibit spatially structured genetic diversity on a regional scale in China. SARS-CoV-2 itself is not a recombinant of any sarbecoviruses detected to date, and its receptor-binding motif, important for specificity to human ACE2 receptors, appears to be an ancestral trait shared with bat viruses and not one acquired recently via recombination. To employ phylogenetic dating methods, recombinant regions of a 68-genome sarbecovirus alignment were removed with three independent methods. Bayesian evolutionary rate and divergence date estimates were shown to be consistent for these three approaches and for two different prior specifications of evolutionary rates based on HCoV-OC43 and MERS-CoV. Divergence dates between SARS-CoV-2 and the bat sarbecovirus reservoir were estimated as 1948 (95% highest posterior density (HPD): 1879-1999), 1969 (95% HPD: 1930-2000) and 1982 (95% HPD: 1948-2009), indicating that the lineage giving rise to SARS-CoV-2 has been circulating unnoticed in bats for decades.
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“Although the proximal origins are unknown, SARS-CoV-2 is thought to derive from a bat SARS-CoV-related coronavirus with a furin cleavage site that enhances the capacity of the virus to infect human cells.48, 49”
From The Lancet Commission on lessons for the future from the COVID-19 pandemic (2022) · cites this paper as [48]
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“1 The virus spread widely within the Hubei province by mid‐January of 2020 and by early March 2020 it spread to the other parts of the globe and henceforth WHO declared SARS COV‐2 as pandemic.[2]”
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Kawashima, I. Y., Lopez, M. C. N., Cunha, M. D. P., & Hashimoto, R. F. (2022) · Scientific Reports · doi:10.1038/s41598-022-08350-6 · Cited by 4
“The model was then applied for the prediction of the viral hosts involved in the viral replication biology of SARS-CoV-2, using 86 virus sequences retrieved from GenBank at 04-26-2020, all of them isolated from human samples (Dataset-3) and additionally 5 sequences of SARS-CoV-2 related viruses…”
MethodSumathi, S., & Vidhya, S. Y. (2022) · Annals of Phytomedicine An International Journal · doi:10.54085/ap.covid19.2022.11.3.7 · Cited by 4
“It is believed to have originated and rapidly spread from Wuhan, China but it’s origin is still a mystery (Boni et al., 2020; Pooladanda et al ., 2020).”
Agile design and development of a high throughput cobas SARS-CoV-2 RT-PCR diagnostic test
Manohar, C. F., Sun, J., Schlag, P., Santini, C., Fontecha, M., Lötscher, P., Bier, C., Goepfert, K., Duncan, D., Spier, G., et al. (2022) · Heliyon · doi:10.1016/j.heliyon.2022.e10591 · Cited by 4
“SARS-CoV-2 coronavirus belongs to the Sarbecovirus sub-genus, which also includes SARS-CoV and other betacoronaviridae identified in bats [7, 8].”
Rojas-Cruz, A. F., Gallego-Gómez, J. C., & Bermúdez-Santana, C. I. (2022) · RNA Biology · doi:10.1080/15476286.2022.2115750 · Cited by 4
“Although the molecular mechanisms enabling cross-species transmission are not well elucidated, it has been proven that essential proteins under selection tend to increase viral fitness, and repeated transmissions may hasten novel strain emergence [15,16].”
Background“A Primordial Situation”: Metonymical Linkages in US Newspaper Coverage of Wet Markets
Rooney, D. (2022) · Environmental Communication · doi:10.1080/17524032.2022.2125548 · Cited by 4
“At the time of coverage examined, it was suggested that pangolins, one of the most heavily trafficked wild animals in the world, were the probable intermediary host between bats and humans, although this has since been rejected (Boni et al., 2020).”
BackgroundDalton, M., Dougall, P., Darko, F. L. A., Annan, W. E., Asante-Asamani, E. O., Bailey, S., Greene, J. M., & White, D. (2022) · PLoS ONE · doi:10.1371/journal.pone.0274407 · Cited by 4
“Coronavirus is the name given to a family of viruses with a characteristic spiked protein protrusion structure that resembles the solar corona [1].”
Bhattacharjee, M. J., Bhattacharya, A., Kashyap, B., Taw, M. J., Li, W., Mukherjee, A. K., & Khan, M. R. (2023) · Virology Journal · doi:10.1186/s12985-023-02139-3 · Cited by 4
“This is consistent with the previous reports that the evolution of SARS-CoV2 variants involved repeated episodes of recombination [20–22].”
ResultDesign, structure and plasma binding of ancestral β-CoV scaffold antigens
Hueting, D., Schriever, K., Sun, R., Vlachiotis, S., Zuo, F., Du, L., Persson, H., Hofström, C., Ohlin, M., Wallden, K., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-42200-x · Cited by 4
Ose, N. J., Campitelli, P., Modi, T., Kazan, I. C., Kumar, S., & Ozkan, S. B. (2023) · eLife · doi:10.7554/elife.92063 · Cited by 9
Li, K., Huntwork, R. H. C., Horn, G. Q., Abraha, M., Hastie, K. M., Li, H., Rayaprolu, V., Olmedillas, E., Feeney, E., Cronin, K. D., et al. (2023) · Journal of Virology · doi:10.1128/jvi.01070-23 · Cited by 4
Seyran, M., Hassan, S. S., Uversky, V. N., Choudhury, P. P., Uhal, B. D., Lundstrom, K. H., Attrish, D., Rezaei, N., Aljabali, A. A. A., Ghosh, S., et al. (2021) · Biomolecules · doi:10.3390/biom11030398 · Cited by 4
“These analyzed sequences are an insufficient representation of all genetically related sarbecoviruses to SARS-CoV-2 in Southeast Asia [1,3,13].”
BackgroundLisewski, A. M. (2022) · F1000Research · doi:10.12688/f1000research.72956.3 · Cited by 4
A Review on COVID-19 Diagnosis Tests Approved for Use in Brazil and the Impact on Pandemic Control
Vedova-Costa, J. M. D., Ramos, E. L. P., Boschero, R. A., Ferreira, G. N., Thomaz‐Soccol, V., Hospinal-Santiani, M., Pacce, V. D., Lustosa, B. P. R., Vicente, V. A., & Soccol, C. R. (2021) · Brazilian Archives of Biology and Technology · doi:10.1590/1678-4324-75years-2021200147 · Cited by 4
From SARS to COVID-19: lessons we should have learned (but we did not)
Lopes, L. R., Campos, J. H. C., & Chaves, A. F. A. (2021) · Journal of Evidence-Based Healthcare · doi:10.17267/2675-021xevidence.2021.e3837 · Cited by 4
SARS-COV-2 EM CÃES E GATOS – REVISÃO DE LITERATURA
de Oliveira, M. C., Gonçalves, N. R., Ferreira, P. D. C., Honório, A. D. S., & de Morais, N. A. (2022) · Veterinária e Zootecnia · doi:10.35172/rvz.2022.v29.676 · Cited by 4
Epizootic, Endemic and Pandemic Zoonotic Viral Infections
Rathore, S. S., Gehlot, H., Prakash, G., & Nandi, J. S. (2022) · Journal of Biosciences and Medicines · doi:10.4236/jbm.2022.103010 · Cited by 4
Lisewski, A. M. (2021) · F1000Research · doi:10.12688/f1000research.72956.1 · Cited by 4
Roche, R., Odeh, N., Andar, A. U., Tulapurkar, M. E., & Roche, J. A. (2023) · Microorganisms · doi:10.3390/microorganisms11081963 · Cited by 4
Abraham, P., Cherian, S., & Potdar, V. A. (2020) · The Indian Journal of Medical Research · doi:10.4103/ijmr.ijmr_3667_20 · Cited by 4
Generation of restriction endonucleases barcode map to trace SARS-CoV-2 origin and evolution
Colombo, F., Corsiero, E., Lewis, M., & Pitzalis, C. (2021) · Scientific Reports · doi:10.1038/s41598-021-91264-6 · Cited by 4
Chiara, M., Horner, D. S., Gissi, C., & Pesole, G. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.06.26.172924 · Cited by 4
“years ago [63].”
Ghafari, M., Hejazi, B., Karshenas, A., Dascalu, S., Luca Ferretti, A., Ledda, A., Khosravi, M. A., Abbasalipour, M., Zeinali, S., & Katzourakis, A. (2020) · doi:10.21203/rs.3.rs-32500/v1 · Cited by 4
Olson, E. J., Brown, D., Chang, T. Z., Ding, L., Ng, T. L., Weiss, H. S., Koide, Y., Koch, P., Rollins, N. J., Mach, P., et al. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.03.02.433434 · Cited by 4
Super-immunity by broadly protective nanobodies to sarbecovirusesPreprint
Xiang, Y., Huang, W., Liu, H., Sang, Z., Nambulli, S., Tubiana, J., Williams, K. L., Duprex, W. P., Schneidman‐Duhovny, D., Wilson, I. A., et al. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.12.26.474192 · Cited by 4
Three-pronged pandemic prevention
(2020) · Nature Ecology & Evolution · doi:10.1038/s41559-020-01304-z · Cited by 4
Removal of Extracellular Vimentin in Blood Confers Resistance to Viral InfectionPreprint
Kim, H.-M., Wang, M., Kim, S., Park, J., & Hong, S. (2022) · Research Square · doi:10.21203/rs.3.rs-2345254/v1 · Cited by 4
The Batalogue: an overview of betacoronaviruses with future pandemic potential
Baird, S., Holmes, E. C., Ashley, C. L., Triccas, J. A., & Steain, M. C. (2025) · FEMS Microbiology Reviews · doi:10.1093/femsre/fuaf023 · Cited by 4
“RaTG13 shares 96.2% nucleotide identity across the whole-genome with SARS-CoV-2, 92.9% in the S gene, but only 89.3% in the RBD (Boni et (Li et al. 2023 ).”
InfluentialComprehensive review on COVID-19: etiology, pathogenicity, and treatment
Zawily, A. E., Eckert, S., Adajar, R. C., Wagih, N., Elmaidomy, A. H., Helmy, A. M., Mustafa, M., Elshorbagi, M., Ghali, E., Fadl, R. G., et al. (2025) · Frontiers in Medicine · doi:10.3389/fmed.2025.1569013 · Cited by 4
A Critical Analysis of the Evidence for the SARS-CoV-2 Origin Hypotheses
Alwine, J. C., Casadevall, A., Enquist, L. W., Goodrum, F. D., & Imperiale, M. J. (2023) · mSphere · doi:10.1128/msphere.00119-23 · Cited by 7
“245 Recombination within the Sarbecovirus subgenus to which SARS-CoV-2 belongs 246 is exceedingly common (18, 22, 23).”
BackgroundBadary, O. A. (2023) · Reviews in Medical Virology · doi:10.1002/rmv.2417 · Cited by 3
“Wuhan, China, in December 2019, as the cause of a pneumonia of unknown aetiology.(1) The SARS‐CoV‐2 rapidly spread all over the globe and on 11 March 2020, the WHO declared COVID‐19 as a global pandemic.”
BackgroundWeller, B., Lin, C., Pogoutse, O., Sauer, M., la Rosa, N. M., Strobel, A., Young, V., Knapp, J. J., Rayhan, A., Falter, C., et al. (2023) · G3 Genes Genomes Genetics · doi:10.1093/g3journal/jkad105 · Cited by 3
Patiño-Galindo, J. Á., García‐Sastre, A., Kuhn, J. H., Rabadán, R., & Palacios, G. F. (2024) · Journal of Virology · doi:10.1128/jvi.01100-24 · Cited by 3
Auffray, C., Balling, R., Blomberg, N., Bonaldo, M. C., Boutron, B., Brahmachari, S. K., Bréchot, C., Cesario, A., Chen, S., Clément, K., et al. (2020) · F1000Research · doi:10.12688/f1000research.26098.1 · Cited by 3
[Origin of SARS-CoV-2 theories, keys and unknowns of an emerged disease.]
Reboredo, R. M. E. (2020) · PubMed Central · Cited by 3
Viral zoom: COVID-19 as multi-scalar immune failure
Horton, Z. (2020) · International Journal of Performance Arts and Digital Media · doi:10.1080/14794713.2020.1827205 · Cited by 3
Los murciélagos y la COVID-19, una injusta historia
Galindo-González, J. R., & Medellín, R. A. (2021) · CIENCIA ergo sum · doi:10.30878/ces.v28n2a10 · Cited by 3
The sudden appearance of SARS-CoV-2
Hidalgo, J., Rodriguez-Vega, G. M., & Pérez-Fernández, J. (2021) · Elsevier eBooks · doi:10.1016/b978-0-323-82860-4.00004-5 · Cited by 5
Jahan, M., Nasif, M. A. O., Rahmat, R., Islam, S. R. U., Munshi, S. U., & Ahmed, M. S. (2022) · Microbiology Resource Announcements · doi:10.1128/mra.00381-22 · Cited by 3
“The causative organism severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) is a member of the Betacoronavirus genus in the Coronaviridae family that also contains other human pathogens, SARS-CoV and MERS-CoV (3, 4).”
BackgroundToehold-controlled ligation and transcription for accurate COVID-19 genotyping
Gao, Y., Wang, T., Li, J. J., Wei, Y., & Qi, H. (2022) · Analytical Biochemistry · doi:10.1016/j.ab.2022.114803 · Cited by 3
Metadata
- Authors
- Boni, M. F., Lemey, P., Jiang, X., Lam, T. T.-Y., Perry, B. W., Castoe, T. A., Rambaut, A., & Robertson, D. L.
- Affiliations
- Pennsylvania State University (US)
- KU Leuven (BE)
- Xi’an Jiaotong-Liverpool University (CN)
- University of Hong Kong (HK)
- The University of Texas at Arlington (US)
- University of Edinburgh (GB)
- MRC University of Glasgow Centre for Virus Research (GB)
- Corresponding author
- Boni, Maciej F.
- Lemey, Philippe
- Rambaut, Andrew
- Robertson, David L.
- ORCID
- Venue
- Nature Microbiology
- Published
- 2020-07-28
- Volume
- 5
- Issue
- 11
- Pages
- 1408-1417
- ISSN
- 2058-5276 (ISSN-L)
- OpenAlex
- W3046218112
- Cited by
- 1,014
- References
- 69
- Citations by year
- 2026: 23 · 2025: 46 · 2024: 79 · 2023: 118 · 2022: 240 · 2021: 327 · 2020: 178
- FWCI
- 28.54
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Nature Microbiology (publishedVersion)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc)
- PubMed (publishedVersion)
- ENLIGHTEN (Jurnal Bimbingan dan Konseling Islam) (submittedVersion, cc-by-sa)
- Lirias (KU Leuven) (submittedVersion)
- Edinburgh Research Explorer (University of Edinburgh) (submittedVersion, other-oa)
- Funders
- Fonds Wetenschappelijk Onderzoek (G0D5117N, G0B9317N)
- Wellcome Trust (206298/Z/17/Z)
- RCUK | Medical Research Council (MC_UU_1201412)
- Topics
- Health Sciences › Medicine › Infectious Diseases › SARS-CoV-2 and COVID-19 Research
- Life Sciences › Agricultural and Biological Sciences › Animal Science and Zoology › Animal Virus Infections Studies
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
- Keywords
- SARS-CoV-2, sarbecoviruses, COVID-19 pandemic, viral recombination, bat reservoirs, pangolins, divergence time estimation, receptor-binding motif, ACE2 receptor, phylogenetic dating, viral emergence, genetic diversity, SARS-CoV
- MeSH terms
- Betacoronavirus, Angiotensin-Converting Enzyme 2, COVID-19, SARS-CoV-2, Animals, Bayes Theorem, China, Chiroptera, Humans, Peptidyl-Dipeptidase A, Phylogeny, Pneumonia, Viral, Recombination, Genetic, Genetic Variation, Genome, Viral, Coronavirus Infections, Evolution, Molecular, Pandemics
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.
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