Cited by 1,014SARS-CoV-2 and COVID-19 ResearchAnimal Virus Infections StudiesEvolution and Genetic Dynamics

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Evolutionary origins of the SARS-CoV-2 sarbecovirus lineage responsible for the COVID-19 pandemic

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Boni, Maciej F., Lemey, Philippe, Jiang, Xiaowei, Lam, Tommy Tsan-Yuk, Perry, Blair W., Castoe, Todd A., Rambaut, Andrew, Robertson, David L.·2020·Nature Microbiology

DOI 10.1038/s41564-020-0771-4

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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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Background
First direct human‐to‐cat transmission of the SARS‐CoV ‐2 B.1.1.7 variant
Çürükoğlu, A., Ergören, M. Ç., Ozgencil, F., Sayıner, S., İNCE, M. E., & Şanlıdağ, T. (2021) · Australian Veterinary Journal · doi:10.1111/avj.13109 · Cited by 19
“Despite the lack of molecular evidence, its particular binding capacity to host human angiotensin-converting enzyme 2 (ACE2) receptor indicates that it originated from common ancestral with severe SARS-like bat coronaviruses.(4,5)”
Background
Keeping up with the COVID's—Could siRNA‐based antivirals be a part of the answer?
Forgham, H., Käkinen, A., Qiao, R., & Davis, T. P. (2022) · Exploration · doi:10.1002/exp.20220012 · Cited by 18
Influenza A(H11N2) Virus Detection in Fecal Samples from Adélie ( Pygoscelis adeliae ) and Chinstrap ( Pygoscelis antarcticus ) Penguins, Penguin Island, Antarctica
Ogrzewalska, M., Motta, F. C., Resende, P. C., Fumian, T. M., da Mendonça, A. C. F., Reis, L. A., Brandão, M. L., Chame, M., Arantes, I., & Siqueira, M. M. (2022) · Microbiology Spectrum · doi:10.1128/spectrum.01427-22 · Cited by 19
Crystal structure of the CoV-Y domain of SARS-CoV-2 nonstructural protein 3
Li, Y., Pustovalova, Y. E., Shi, W., Gorbatyuk, O., Sreeramulu, S., Schwalbe, H., Hoch, J. C., & Hao, B. (2023) · Scientific Reports · doi:10.1038/s41598-023-30045-9 · Cited by 20
Rapid genomic surveillance of SARS-CoV-2 in a dense urban community of Kathmandu Valley using sewage samples
Napit, R., Manandhar, P., Chaudhary, A., Shrestha, B., Poudel, A., Raut, R., Pradhan, S. M., Raut, S., Rajbhandari, P. G., Gurung, A., et al. (2023) · PLoS ONE · doi:10.1371/journal.pone.0283664 · Cited by 19
Molecular Diagnostic Tools for the Detection of SARS-CoV-2
Datta, M., Singh, D. D., & Naqvi, A. R. (2021) · International Reviews of Immunology · doi:10.1080/08830185.2020.1871477 · Cited by 20
The pigtail macaque (Macaca nemestrina) model of COVID-19 reproduces diverse clinical outcomes and reveals new and complex signatures of disease
Melton, A., Doyle‐Meyers, L. A., Blair, R. V., Midkiff, C. C., Melton, H. J., Russell‐Lodrigue, K., Aye, P. P., Schiro, F. R., Fahlberg, M. D., Szeltner, D. M., et al. (2021) · PLoS Pathogens · doi:10.1371/journal.ppat.1010162 · Cited by 19
Coronavirus (COVID-19): A Systematic Review and Meta-analysis to Evaluate the Significance of Demographics and ComorbiditiesPreprint
Bhattacharyya, A., Seth, A. K., Srivast, N., Imeokparia, M., & Rai, S. N. (2021) · Research Square · doi:10.21203/rs.3.rs-144684/v1 · Cited by 17
SARS-CoV-2: The Interplay Between Evolution and Host Immunity
Case, J. B., Jain, S., Suthar, M. S., & Diamond, M. (2024) · Annual Review of Immunology · doi:10.1146/annurev-immunol-083122-043054 · Cited by 26
“Although multiple studies suggest that recombination between a pangolin CoV (Pang/GD) and a bat CoV (RaTG13) facilitated the emergence of SARS-CoV-2 (131, 132), others argue that recombination was not the primary evolutionary mechanism (133–135).”
Exploring the immuno-nano nexus: A paradigm shift in tumor vaccines
Li, Y., Xu, Y., Su, W., Xu, J., Ye, Z., Wang, Z., Liu, Q., & Chen, F. (2025) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2025.117897 · Cited by 18
Comparative Study of COVID-19 Pandemic Progressions in 175 Regions in Australia, Canada, Italy, Japan, Spain, U.K. and USA Using a Novel Model That Considers Testing Capacity and Deficiency in Confirming Infected Cases
Zhan, C., Tse, C. K., Gao, Y., & Hao, T. (2021) · IEEE Journal of Biomedical and Health Informatics · doi:10.1109/jbhi.2021.3089577 · Cited by 18
“THE Novel Coronavirus Disease 2019 (COVID-19), caused by severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) [1] which has a long evolutionary history in bats [2], began to spread in China since December 2019 and was found to be highly contagious with a reproductive number as high as 6.”
Background
Physiology and ecology combine to determine host and vector importance for Ross River virus
Kain, M. P., Skinner, E. B., van den Hurk, A. F., McCallum, H. I., & Mordecai, E. A. (2021) · eLife · doi:10.7554/elife.67018 · Cited by 18
Serum Proteomics Identifies Immune Pathways and Candidate Biomarkers of Coronavirus Infection in Wild Vampire Bats
Becker, D. J., Lei, G.-S., Janech, M. G., Bland, A. M., Fenton, M. B., Simmons, N. B., Relich, R. F., & Neely, B. A. (2022) · Frontiers in Virology · doi:10.3389/fviro.2022.862961 · Cited by 15
“, SARS-CoV, MERS-CoV, SARS-CoV-2) have also been ascribed to bats, but spillover has typically involved intermediate hosts rather than direct bat-to-human transmission (5, 29, 30).”
Background
Tracing the origin of Severe acute respiratory syndrome coronavirus‐2 (SARS‐CoV‐2): A systematic review and narrative synthesis
Thakur, N. N., Das, S., Kumar, S., Maurya, V. K., Dhama, K., Paweska, J. T., Abdel-Moneim, A. S., Jain, A., Tripathi, A. K., Puri, B., et al. (2022) · Journal of Medical Virology · doi:10.1002/jmv.28060 · Cited by 17
MHC class II genes mediate susceptibility and resistance to coronavirus infections in bats
Schmid, D. W., Meyer, M., Wilhelm, K., Tilley, T., Link‐Hessing, T., Fleischer, R., Badu, E. K., Nkrumah, E. E., Oppong, S. K., Schwensow, N., et al. (2023) · Molecular Ecology · doi:10.1111/mec.16983 · Cited by 19
Phylogeography of horseshoe bat sarbecoviruses in Vietnam and neighbouring countries. Implications for the origins of SARS ‐ CoV and SARS ‐ CoV ‐2
Hassanin, A., Tú, V. T., Görföl, T., LAM, N. Q., Pham, P. V., Hang, C. T., Tuấn, T. A., Prot, M., Simon‐Lorière, E., Kemenesi, G., et al. (2024) · Molecular Ecology · doi:10.1111/mec.17486 · Cited by 19
“Importantly, both F486L and Q498H mutations were detected in SARS- CoV-2 during the COVID-19 pandemic, and neither was found to have a nega - tive effect on the binding affinity of RBD to human ACE2 (Huang et al., 2021; Zhou et al., 2022 ).”
Influential
Structural Dynamics and Molecular Evolution of the SARS-CoV-2 Spike Protein
Wolf, K., Kwan, J. C., & Kamil, J. P. (2022) · mBio · doi:10.1128/mbio.02030-21 · Cited by 17
DGraph Clusters Flaviviruses and β-Coronaviruses According to Their Hosts, Disease Type, and Human Cell Receptors
Braun, B. A., Schein, C. H., & Braun, W. A. (2021) · Bioinformatics and Biology Insights · doi:10.1177/11779322211020316 · Cited by 18
Diverse hosts, diverse immune systems: Evolutionary variation in bat immunology
Becker, D. J., Vicente‐Santos, A., Reers, A. B., Ansil, B. R., O'Shea, M., Cummings, C. A., Roistacher, A., Quintela‐Tizon, R. M., Pereira, M. M. T., Rosen, J., et al. (2025) · Annals of the New York Academy of Sciences · doi:10.1111/nyas.15395 · Cited by 17
“268,269 To statistically differentiate multiple, competing evolutionary hypotheses about the drivers of interspecific variation in bat immunology, we suggest greater adoption of frameworks for causal inference, 270,271 such as causal mediation analysis (CMA).”
A recent origin of Orf3a from M protein across the coronavirus lineage arising by sharp divergence
Ouzounis, C. A. (2020) · Computational and Structural Biotechnology Journal · doi:10.1016/j.csbj.2020.11.047 · Cited by 17
“Other animal groups such as pangolins [8] have also been considered as reservoir species, based on irregularities or recombination events [6,9] for parts of certain genes and the genome.”
In silico Analysis of SARS-CoV-2 ORF8-Binding Proteins Reveals the Involvement of ORF8 in Acquired-Immune and Innate-Immune Systems
Takatsuka, H., Fahmi, M., Hamanishi, K., Sakuratani, T., Kubota, Y., & Ito, M. (2022) · Frontiers in Medicine · doi:10.3389/fmed.2022.824622 · Cited by 17
Modeling the evolution of SARS-CoV-2 under non-pharmaceutical interventions and testing
Gurevich, Y., Ram, Y., & Hadany, L. (2022) · Evolution Medicine and Public Health · doi:10.1093/emph/eoac013 · Cited by 12
Natural reservoir Rousettus aegyptiacus bat host model of orthonairovirus infection identifies potential zoonotic spillover mechanisms
Schuh, A. J., Amman, B. R., Guito, J. C., Graziano, J. C., Sealy, T. K., Kirejczyk, S. G. M., & Towner, J. S. (2022) · Scientific Reports · doi:10.1038/s41598-022-24673-w · Cited by 17
Developing an appropriate evolutionary baseline model for the study of SARS-CoV-2 patient samples
Terbot, J. W., Johri, P., Liphardt, S. W., Soni, V., Pfeifer, S. P., Cooper, B. S., Good, J. M., & Jensen, J. D. (2023) · PLoS Pathogens · doi:10.1371/journal.ppat.1011265 · Cited by 16
An immediate way to lower pandemic risk: (not) seizing the low-hanging fruit (bat)
Osofsky, S. A., Lieberman, S., Walzer, C., Lee, H. L., & Neme, L. A. (2023) · The Lancet Planetary Health · doi:10.1016/s2542-5196(23)00077-3 · Cited by 19
Newly identified lineages of porcine hemagglutinating encephalomyelitis virus exhibit respiratory phenotype
He, W., Li, D., Baele, G., Zhao, J., Jiang, Z., Ji, X., Veit, M., Suchard, M. A., Holmes, E. C., Lemey, P., et al. (2023) · Virus Evolution · doi:10.1093/ve/vead051 · Cited by 17
Self-citation
Bat Ecology and Microbiome of the Gut: A Narrative Review of Associated Potentials in Emerging and Zoonotic Diseases
Bazzoni, E., Cacciotto, C., Zobba, R., Pittau, M., Martella, V., & Alberti, A. (2024) · Animals · doi:10.3390/ani14203043 · Cited by 17
Molecular epidemiology in the HIV and SARS-CoV-2 pandemics
Lorenzo-Redondo, R., Ozer, E. A., Achenbach, C. J., D’Aquila, R. T., & Hultquist, J. F. (2020) · Current Opinion in HIV and AIDS · doi:10.1097/coh.0000000000000660 · Cited by 21
“Relative to HIV, however, the low mutation rate of SARS-CoV-2 somewhat tempers these concerns [69,70].”
Background
Evaluating the effectiveness of control measures in multiple regions during the early phase of the COVID-19 pandemic in 2020
Wang, Z., Whittington, J. D., Yuan, H., Miao, H., Tian, H., & Stenseth, N. C. (2021) · Biosafety and Health · doi:10.1016/j.bsheal.2021.09.002 · Cited by 16
“2% [147], there is a possibility of decades of evolutionary divergence between them [148].”
SARS-CoV-2: An Overview of the Genetic Profile and Vaccine Effectiveness of the Five Variants of Concern
Dumache, R., Enache, A., Macasoi, I. G., Dehelean, C. A., Dumitrascu, V. C., Mihailescu, A., Popescu, R., Vlad, M., Vlad, C. S., & Mureşan, C. O. (2022) · Pathogens · doi:10.3390/pathogens11050516 · Cited by 17
“The evolutionary history of the S protein is complex, the sequence of this protein being composed of several segments that are phylogenetically related to the different strains of Sarbecovirus [70].”
Background
Delta Variant with P681R Critical Mutation Revealed by Ultra-Large Atomic-Scale Ab Initio Simulation: Implications for the Fundamentals of Biomolecular Interactions
Adhikari, P., Jawad, B., Rao, P. R., Podgornik, R., & Ching, W. Y. (2022) · Viruses · doi:10.3390/v14030465 · Cited by 14
“SARS-CoV-2 itself is most likely the result of a recombination between different SARS-related coronaviruses [61], with different subsequent mutations affecting their many biological and biomedical properties, such as pathogenicity, infectivity, transmissibility, and/or antigenicity, even though they tend to be either…”
Background
European context of the diversity and phylogenetic position of SARS-CoV-2 sequences from Polish COVID-19 patients
Hryhorowicz, S., Ustaszewski, A., Kaczmarek-Ryś, M., Lis, E., Witt, M., Pławski, A., & Ziętkiewicz, E. (2021) · Journal of Applied Genetics · doi:10.1007/s13353-020-00603-2 · Cited by 15
“…is believed to underlie evolutionary jumps, which allow viruses to change their hosts (Su et al. 2016; Luk et al. 2019), the role of the present knowledge does not allow to assess whether recombination plays any role in SARS-CoV-2 acquiring specificity for human ACE2 receptor (Boni et al. 2020).”
Background
COVID-19: Auswirkungen auf Lunge und Herz
Ackermann, M., Werlein, C., Länger, F. P., Kühnel, M., & Jonigk, D. D. (2021) · Der Pathologe · doi:10.1007/s00292-021-00918-9 · Cited by 16
Estimating the age of the subfamily Orthocoronavirinae using host divergence times as calibration ages at two internal nodes
Hayman, D. T. S., & Knox, M. A. (2021) · Virology · doi:10.1016/j.virol.2021.08.004 · Cited by 16
“When clocks become unreliable, therefore, is unknown, though clearly analyses of more recent ancestries like SARS-coronaviruses are most reliable of all (Boni et al., 2020).”
Background
Structural basis of SARS-CoV-2 and its variants binding to intermediate horseshoe bat ACE2
Tang, L., Zhang, D., Han, P., Kang, X., Zheng, A., Xu, Z., Zhao, X., Wang, V. Y., Qi, J., Wang, Q., et al. (2022) · International Journal of Biological Sciences · doi:10.7150/ijbs.73640 · Cited by 16
“Bats are identified as reservoir hosts of CoVs, some of which are closely related to SARS-CoV or SARS-CoV-2 [11, 28-32], two important humaninfecting CoVs.”
BackgroundMethod
SARS-COV-2/COVID-19: scenario, epidemiology, adaptive mutations, and environmental factors
Asghar, A., Imran, H. M., Bano, N., Maalik, S., Mushtaq, S., Hussain, A., Varjani, S., Aleya, L., Iqbal, H. M. N., & Bilal, M. (2022) · Environmental Science and Pollution Research · doi:10.1007/s11356-022-22333-0 · Cited by 16
“Long-term genetic studies across more distantly related coronavirus lineages show that detrimental mutations are anticipated to be eliminated (Boni et al. 2020).”
Background
Viral infections at the animal–human interface—Learning lessons from the SARS‐CoV ‐2 pandemic
Brüssow, H. (2023) · Microbial Biotechnology · doi:10.1111/1751-7915.14269 · Cited by 17
Clinical validation of automated and rapid mariPOC SARS-CoV-2 antigen test
Koskinen, J. M., Antikainen, P., Hotakainen, K., Haveri, A., Ikonen, N., Savolainen‐Kopra, C., Sundström, K., & Koskinen, J. O. (2021) · Scientific Reports · doi:10.1038/s41598-021-99886-6 · Cited by 16
Comparative phylogenetic analysis of SARS-CoV-2 spike protein—possibility effect on virus spillover
Ghorbani, A., Samarfard, S., Eskandarzade, N., Afsharifar, A., Eskandari, M. H., Niazi‎, A., Izadpanah, K., & Karbanowicz, T. P. (2021) · Briefings in Bioinformatics · doi:10.1093/bib/bbab144 · Cited by 18
From Protein to Pandemic: The Transdisciplinary Approach Needed to Prevent Spillover and the Next Pandemic
Plowright, R. K., & Hudson, P. J. (2021) · Viruses · doi:10.3390/v13071298 · Cited by 16
Independent acquisition of short insertions at the RIR1 site in the spike N‐terminal domain of the SARS‐CoV‐2 BA.2 lineage
Greco, S., & Gerdol, M. (2022) · Transboundary and Emerging Diseases · doi:10.1111/tbed.14672 · Cited by 17
No detectable signal for ongoing genetic recombination in SARS-CoV-2Preprint
Richard, D., Owen, C. J., van Dorp, L., & Balloux, F. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.12.15.422866 · Cited by 15
Can Science Help Resolve the Controversy on the Origins of the SARS-CoV-2 Pandemic?
Casadevall, A., Weiss, S. R., & Imperiale, M. J. (2021) · mBio · doi:10.1128/mbio.01948-21 · Cited by 16
“Here, one would need to define “close” since wild coronaviruses are already 95% similar in sequence and relatives of SARSCoV-2 are already known to be circulating in animals (1, 17).”
Background
Conserved molecular signatures in the spike protein provide evidence indicating the origin of SARS-CoV-2 and a Pangolin-CoV (MP789) by recombination(s) between specific lineages of Sarbecoviruses
Gupta, R. S., & Khadka, B. (2021) · PeerJ · doi:10.7717/peerj.12434 · Cited by 15
Investigations on SARS-CoV-2 Susceptibility of Domestic and Wild Animals Using Primary Cell Culture Models Derived from the Upper and Lower Respiratory Tract
Färber, I., Krüger, J., Rocha, C., Armando, F., von Köckritz‐Blickwede, M., Pöhlmann, S., Braun, A. C., Baumgärtner, W., Runft, S., & Krüger, N. (2022) · Viruses · doi:10.3390/v14040828 · Cited by 14
Mosaic Recombination Inflicted Various SARS-CoV-2 Lineages to Emerge into Novel Virus Variants: a Review Update
Singh, P., Sharma, K. K., Shaw, D., Bhargava, A., & Negi, S. S. (2022) · Indian Journal of Clinical Biochemistry · doi:10.1007/s12291-022-01109-w · Cited by 15
“SARS-CoV-2 also has the positive-sense and non-segment RNA genome, so the appearance of the different variants has drawn the attention of the scientific community to the role of recombination in the emergence of recombinant lineages of the virus[25].”
Background
Determinants of species-specific utilization of ACE2 by human and animal coronaviruses
Wang, Q., Noettger, S., Xie, Q., Pastorio, C., Seidel, A., Müller, J. A., Jung, C., Jacob, T., Sparrer, K. M. J., Zech, F., et al. (2023) · Communications Biology · doi:10.1038/s42003-023-05436-3 · Cited by 15
Therapeutic antibodies and alternative formats against SARS-CoV-2
Winiger, R. R., & Perez, L. H. (2024) · Antiviral Research · doi:10.1016/j.antiviral.2024.105820 · Cited by 16
Recombination should not be an afterthought
Neches, R. Y., McGee, M. D., & Kyrpides, N. C. (2020) · Nature Reviews Microbiology · doi:10.1038/s41579-020-00451-1 · Cited by 15

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: Boni, Maciej F.
Lemey, Philippe
Jiang, Xiaowei
Lam, Tommy Tsan-Yuk
Perry, Blair W.
Castoe, Todd A.
Rambaut, Andrew
Robertson, David L.
Venue: Nature Microbiology
Publisher: Springer Science and Business Media LLC
Published: 2020-07-28
Volume: 5
Issue: 11
Pages: 1408-1417
ISSN: 2058-5276 (ISSN-L)
DOI: 10.1038/s41564-020-0771-4
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: www.springernature.com/gp/researchers/text-and-data-mining (tdm)
www.springernature.com/gp/researchers/text-and-data-mining (vor)
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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Evolutionary origins of the SARS-CoV-2 sarbecovirus lineage responsible for the COVID-19 pandemic

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