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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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Chan, A. P.-Y., Siddique, A., Desplat, Y., Choi, Y., Ranganathan, S., Choudhary, K. S., Khalid, M. F., Diaz, J., Bezney, J., DeAscanis, D., et al. (2023) · Cell Reports Methods · doi:10.1016/j.crmeth.2023.100463 · Cited by 16
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MethodSARS-CoV-2 Portrayed against HIV: Contrary Viral Strategies in Similar Disguise
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Apaa, T., Withers, A. J., Staley, C. E., Blanchard, A. M., Bennett, M., Bremner‐Harrison, S., Chadwick, E. A., Hailer, F., Harrison, S. W. R., Loose, M., et al. (2023) · Journal of General Virology · doi:10.1099/jgv.0.001859 · Cited by 11
Bat-Borne Coronaviruses in Jordan and Saudi Arabia: A Threat to Public Health?
AL-Eitan, L. N., Tarkhan, A. H., Alghamdi, M. A., Marston, D. A., Wu, G., McElhinney, L. M., Brown, I. H., & Fooks, A. R. (2020) · Viruses · doi:10.3390/v12121413 · Cited by 11
“However, at this point in time, there is no reliable information on the potential intermediate hosts of SARS-CoV-2, or even if an intermediate host was required [175,176].”
BackgroundBamford, C., Broadbent, L., Aranday-Cortés, E., McCabe, M., McKenna, J. P., Courtney, D., Touzelet, O., Ali, A., Roberts, G. C., López–Campos, G., et al. (2022) · Viruses · doi:10.3390/v14020325 · Cited by 12
“Reflecting its likely zoonotic origins, SARS-CoV-2-like and other SARS-related viruses have been detected and isolated from horseshoe bats and pangolins from Asia [4].”
BackgroundVaggu, R. G., Chakraborty, R., Chakraborty, A., Lavudi, K., Patnaik, S., Sharma, S., & Patnaik, S. (2022) · Computers in Biology and Medicine · doi:10.1016/j.compbiomed.2022.105436 · Cited by 10
“In fact, there have been evidences to showing that in the viral lineage, this protein is an evolutionary hot spot [27,32].”
SARS-CoV-2 gained a novel spike protein S1–N-Terminal Domain (S1-NTD)
Desingu, P. A., Nagarajan, K., & Dhama, K. (2022) · Environmental Research · doi:10.1016/j.envres.2022.113047 · Cited by 11
Molecular characterization of a new SARS-CoV-2 recombinant cluster XAG identified in Brazil
Silva, T. D. S., Salvato, R. S., Gregianini, T. S., Arantes, I., Pereira, E. C., de Oliveira, E., de Menezes, A. L., Barcellos, R. B., Godinho, F. M. D. S., Riediger, I. N., et al. (2022) · Frontiers in Medicine · doi:10.3389/fmed.2022.1008600 · Cited by 11
“Coronaviruses (CoVs) are highly recombinogenic, unlike other viruses that have emerged in the past two decades (27).”
BackgroundA SARS-CoV-2: Companion Animal Transmission and Variants Classification
Pandit, R., & Matthews, Q. L. (2023) · Pathogens · doi:10.3390/pathogens12060775 · Cited by 11
Lam, S. D., Bordin, N., Waman, V., Scholes, H. M., Ashford, P., Sen, N., van Dorp, L., Rauer, C., Dawson, N. L., Pang, C., et al. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.05.01.072371 · Cited by 12
The impact of super-spreaders in COVID-19: mapping genome variation worldwidePreprint
Gómez‐Carballa, A., Bello, X., Pardo‐Seco, J., Martinón‐Torres, F., & Salas, A. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.05.19.097410 · Cited by 11
“Divergence dates between SARS-CoV-2 and bat sarbecovirus reservoir and between bat and pangolin coronavirus were taken from (Boni et al. 2020).”
BackgroundHauser, B. M., Sangesland, M., Lam, E. C., Denis, K. S., Feldman, J. E., Yousif, A. S., Caradonna, T. M., Kannegieter, T., Balazs, A. B., Lingwood, D., et al. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.12.07.415216 · Cited by 11
“Indeed, surveillance efforts have 66 identified numerous unique coronaviruses within various animal reservoirs, raising the possibility 67 of zoonotic transmission (2, 3).”
BackgroundThe coevolutionary mosaic of bat betacoronavirus emergence riskPreprint
Forero, N., Muylaert, R. L., Seifert, S. N., Albery, G. F., Becker, D. J., Carlson, C. J., & Poisot, T. (2022) · doi:10.32942/osf.io/8mgv6 · Cited by 11
Çakal, B. (2020) · Turkiye Klinikleri Journal of Medical Ethics-Law and History · doi:10.5336/mdethic.2020-76286 · Cited by 10
Conservation and cultural intersections within Hong Kong's snake soup industry
Yuan, F. L., Yeung, C. T., Prigge, T., Dufour, P. C., Sung, Y., Dingle, C., & Bonebrake, T. C. (2022) · Oryx · doi:10.1017/s0030605321001630 · Cited by 10
A Trait-Based Approach to Predicting Viral Host-Range Evolvability
Strobel, H. M., Stuart, E. C., & Meyer, J. R. (2022) · Annual Review of Virology · doi:10.1146/annurev-virology-091919-092003 · Cited by 12
Su, X., Huang, Z., Xu, W., Wang, Q., Xing, L., Lu, L., Jiang, S., & Xia, S. (2023) · Biomolecules · doi:10.3390/biom13091283 · Cited by 9
“In addition, different SARS-like coronaviruses (SL-CoVs) have been isolated from bats [11], such as SHC014-CoV and WIV1-CoV [12,13], belonging to the Sarbecovirus subgenus of β -CoV, along with SARS-CoV and SARS-CoV-2 [14].”
BackgroundAssessing the emergence time of SARS-CoV-2 zoonotic spillover
Samson, S., Lord, É., & Makarenkov, V. (2024) · PLoS ONE · doi:10.1371/journal.pone.0301195 · Cited by 10
“Furthermore, different coronaviruses are known to evolve at different evolutionary rates [3].”
BackgroundThird update on possible animal sources for human COVID‐19
Opriessnig, T., & Huang, Y. (2021) · Xenotransplantation · doi:10.1111/xen.12671 · Cited by 10
Wiemeyer, G. M., Plaza, P. I., Bustos, C., Muñoz, A. J., & Lambertucci, S. A. (2021) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph18105231 · Cited by 10
“In fact, the pandemic event emerged in 2019, with millions of people being infected and many dying because of SARS-CoV-2 virus, was originated as a spillover probably from bats [3,4].”
BackgroundStatistical Challenges in Tracking the Evolution of SARS-CoV-2
Cappello, L., Kim, J., Liu, S., & Palacios, J. A. (2022) · Statistical Science · doi:10.1214/22-sts853 · Cited by 8
Harfoot, R., Lawley, B., Hernández, L. C., Kuang, J., Grant, J., Treece, J. M., Lequeux, S., Day, R. C., Jack, S. J., Stanton, J. L., et al. (2022) · Viruses · doi:10.3390/v14020366 · Cited by 10
“This vast amount of information has been used to understand the evolution and epidemiology of the virus [8,58,59], leading to the classification of SARS-CoV-2 genetic diversity into clades or lineages [12].”
BackgroundMethodHoberg, E. P., Boeger, W. A., Brooks, D. R., Trivellone, V., & Agosta, S. J. (2022) · MANTER Journal of Parasite Biodiversity · doi:10.32873/unl.dc.manter18 · Cited by 10
Orłowska, A., Smreczak, M., Thor, K. A., Niedbalska, M., Pawelec, D., Trębas, P., & Rola, J. (2022) · Viruses · doi:10.3390/v14091914 · Cited by 10
Irfan, E., Dilshad, E., Ahmad, F., Almajhdi, F. N., Hussain, T., Abdi, G., & Waheed, Y. (2024) · BMC Infectious Diseases · doi:10.1186/s12879-024-09387-w · Cited by 10
“An initial study showed that almost 91% of affected individuals showed high fever, 77% had a cough, 44% individuals felt fatigued, other symptoms like salivation were shown by 28%, headache by 8%, 5% had hemoptysis and 3% faced diarrhea [10].”
BackgroundEl SARS-CoV-2 y otros virus emergentes y su relación con la inocuidad en la cadena alimentaria
Silva-Jaimes, M. I. (2020) · Scientia Agropecuaria · doi:10.17268/sci.agropecu.2020.02.15 · Cited by 12
“La cepa causal del SARS-CoV-2, que hoy nos aqueja trágicamente, podría haberse separado de los coronavirus del murciélago y haber trajinado entre pangolines, serpientes y humanos al menos durante 40 años (Lam et al, 2020; Zhang et al., 2020; Maciej et al. 2020).”
BackgroundVariable routes to genomic and host adaptation among coronaviruses
Montoya, V., McLaughlin, A., Mordecai, G. J., Miller, R. L., & Joy, J. B. (2021) · Journal of Evolutionary Biology · doi:10.1111/jeb.13771 · Cited by 12
“Parallel evolution, well documented throughout the tree of life (Boughman et al., 2005; Nosil et al., 2002; Schluter et al., 2004), has been repeatedly observed in viruses during host shifts both in vitro and in vivo (Bedhomme et al., 2012; Remold et al., 2008; Wichman et al., 1999).”
BackgroundA Perspective on COVID-19 Management
Pavelić, K., Pavelić, S. K., Brix, B., & Goswami, N. (2021) · Journal of Clinical Medicine · doi:10.3390/jcm10081586 · Cited by 12
“Some papers discuss a possible linkage of COVID-19 to coronaviruses, especially to bat coronaviruses where robust data is presented on the similarities between the genetic material of SARS-CoV-2 and other SARS-CoV viruses [10].”
BackgroundGenomic Characterization of a Novel Alphacoronavirus Isolated from Bats, Korea, 2020
Do, H.-Q., Nguyen, V. G., Chung, C., Jeon, Y.-S., Shin, S., Jang, K.-C., Pham, L. B. H., Kong, A., Kim, C.-U., Park, Y., et al. (2021) · Viruses · doi:10.3390/v13102041 · Cited by 10
“Several strains of Alphacoronavirus and Betacoronavirus detected in bats have been known to induce diseases such as COVID-19, responsible for the current pandemic, as well as many serious infectious diseases in livestock [17,18].”
BackgroundGenomic Bootstrap Barcodes and Their Application to Study the Evolution of Sarbecoviruses
Hassanin, A., Rambaud, O., & Klein, D. (2022) · Viruses · doi:10.3390/v14020440 · Cited by 12
“Although two sarbecoviruses were recently discovered in Sunda pangolins (Manis javanaica), all major Viruses 2022, 14, 440. https://doi.org/10.3390/v14020440 https://www.mdpi.com/journal/viruses lineages of Sarbecovirus have been detected in horseshoe bats (Chiroptera, Rhinolophidae, Rhinolophus) [5,6].”
BackgroundMethodResultInfluentialRoy, S., Ghosh, P., Bandyopadhyay, A., & Basu, S. (2022) · Vaccines · doi:10.3390/vaccines10020301 · Cited by 11
“Several theories (or, hypotheses) regarding the origin of SARS-CoV-2 have been advocated, including (but not limited to) engineered viruses, viruses that are naturally in circulation from one host to another, manipulating their hosts for transmission and virulence (the ‘circulation model’) [9], the bat–pangolin recomb…”
BackgroundCoronavirus, capitalism and a ‘thousand tiny dis/advantages’: a more-than-human analysis
Fox, N. J. (2022) · Social Theory & Health · doi:10.1057/s41285-022-00179-3 · Cited by 11
Gennaro, F. D., & Petrosillo, N. (2022) · Acta otorhinolaryngologica italica · doi:10.14639/0392-100x-suppl.1-42-2022-01 · Cited by 11
Patel, R. S., & Agrawal, B. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.952229 · Cited by 10
“SARS-CoV-2 and RaTG13 diverged more than 30 years ago into two lineages where RaTG13 was a recombinant virus, and SARSCoV-2 possessed the ancestral RBD trait that is shared among bat viruses (15, 16).”
BackgroundRASCL: Rapid Assessment of Selection in CLades through molecular sequence analysis
Lucaci, A. G., Zehr, J. D., Shank, S. D., Bouvier, D., Ostrovsky, A., Han, M., Nekrutenko, A., Martin, D. P., & Pond, S. L. K. (2022) · PLoS ONE · doi:10.1371/journal.pone.0275623 · Cited by 10
Ramazzotti, D., Angaroni, F., Maspero, D., Gambacorti-Passerini, C. B., Antoniotti, M., Graudenzi, A., & Piazza, R. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.04.22.044404 · Cited by 12
Detecting punctuated evolution in SARS-CoV-2 over the first year of the pandemic
Surya, K., Gardner, J. D., & Organ, C. L. (2023) · Frontiers in Virology · doi:10.3389/fviro.2023.1066147 · Cited by 9
“(44) (58 from humans and 11 from civets and raccoon dogs).”
BackgroundResultInfluentialGenetic Diversity and Evolution of Viruses Infecting Felis catus: A Global Perspective
Le, S.-J., Xin, G.-Y., Wu, W.-C., & Shī, M. (2023) · Viruses · doi:10.3390/v15061338 · Cited by 9
The comparison of pathogenicity among SARS-CoV-2 variants in domestic cats
Park, E., Kuroda, Y., Uda, A., Kaku, Y., Okutani, A., Hotta, A., Tatemoto, K., Ishijima, K., Inoue, Y., Harada, M., et al. (2024) · Scientific Reports · doi:10.1038/s41598-024-71791-8 · Cited by 9
Antiviral Effects of Avian Interferon-Stimulated Genes
He, X., Zhang, S., Zou, Z., Gao, P., Yang, L., & Xiang, B. (2024) · Animals · doi:10.3390/ani14213062 · Cited by 11
Eldin, P., David, A., Hirtz, C., Battini, J., & Briant, L. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms252111614 · Cited by 9
From viral evolution to spatial contagion: a biologically modulated Hawkes model
Holbrook, A. J., Ji, X., & Suchard, M. A. (2022) · Bioinformatics · doi:10.1093/bioinformatics/btac027 · Cited by 10
Where is echinoderm aquaculture heading in Latin America? Potential, challenges and opportunities.
Sonnenholzner, J. (2021) · Revista de Biología Tropical · doi:10.15517/rbt.v69isuppl.1.46393 · Cited by 9
“Pero, hoy en día la situación de la Pandemia Covid-19 (Boni et al., 2020) ha afectado severamente el desempeño económico de la entera región de América Latina y Caribe (CEPAL, 2020) registrándose un retroceso sin precedente en los últimos cien años (CELAC, 2020; FSIN, 2020), dificultándose la producción de alimentos (…”
BackgroundThe Emergence of the New P.4 Lineage of SARS-CoV-2 With Spike L452R Mutation in Brazil
Bittar, C., Possebon, F. S., Ullmann, L. S., Geraldini, D. B., da Costa, V. G., de Almeida, L. G. P., Sanches, P. R. D. S., Nascimento-Júnior, N. M., Cilli, E. M., Banho, C. Á., et al. (2021) · Frontiers in Public Health · doi:10.3389/fpubh.2021.745310 · Cited by 10
“Molecular data suggest that SARS-CoV2 originated in bats, as has the other Betacoronavirus that cause severe respiratory syndrome SARS-CoV and MERS-CoV, and emerged in humans following passage through an intermediary host (3, 4).”
BackgroundInfluentialPeptide candidates for the development of therapeutics and vaccines against β-coronavirus infection
Chourasia, R., Padhi, S., Phukon, L. C., Abedin, M. M., Sirohi, R., Singh, S. P., & Rai, A. K. (2022) · Bioengineered · doi:10.1080/21655979.2022.2060453 · Cited by 10
“Besides, SARS-CoV-2 shares about 79% and 50% sequence identity with SARS-CoV and MERS-CoV, respectively [11].”
BackgroundInfluentialGenome Structure, Life Cycle, and Taxonomy of Coronaviruses and the Evolution of SARS-CoV-2
Lamkiewicz, K., Gomez, L. R. E., Kühnert, D., & Marz, M. (2023) · Current topics in microbiology and immunology · doi:10.1007/978-3-031-15640-3_9 · Cited by 11
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
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