The emergence and ongoing convergent evolution of the N501Y lineages coincides with a major global shift in the SARS-CoV-2 selective landscape
Open accessPreprint — published as 10.1016/j.cell.2021.09.003
Abstract
The emergence and rapid rise in prevalence of three independent SARS-CoV-2 “501Y lineages’’, B.1.1.7, B.1.351 and P.1, in the last three months of 2020 prompted renewed concerns about the evolutionary capacity of SARS-CoV-2 to adapt to both rising population immunity, and public health interventions such as vaccines and social distancing. Viruses giving rise to the different 501Y lineages have, presumably under intense natural selection following a shift in host environment, independently acquired multiple unique and convergent mutations. As a consequence, all have gained epidemiological and immunological properties that will likely complicate the control of COVID-19. Here, by examining patterns of mutations that arose in SARS-CoV-2 genomes during the pandemic we find evidence of a major change in the selective forces acting on various SARS-CoV-2 genes and gene segments (such as S, nsp2 and nsp6), that likely coincided with the emergence of the 501Y lineages. In addition to involving continuing sequence diversification, we find evidence that a significant portion of the ongoing adaptive evolution of the 501Y lineages also involves further convergence between the lineages. Our findings highlight the importance of monitoring how members of these known 501Y lineages, and others still undiscovered, are convergently evolving similar strategies to ensure their persistence in the face of mounting infection and vaccine induced host immune recognition.
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The Alpha variant contains non-spike mutations including nsp6:Δ106-108 and nucleocapsid mutations D3L, R203K and G204R, which may increase transmission by antagonizing innate immunity.
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MacLean, O. A., Lytras, S., Weaver, S., Singer, J. B., Boni, M. F., Lemey, P., Pond, S. L. K., & Robertson, D. L. (2021) · PLoS Biology · doi:10.1371/journal.pbio.3001115 · Cited by 215 · cited 5× · see citing works
“This behavior is consistent with exponential growth in a population of naive susceptible hosts that do not exert significant selective pressures on the pathogen prior to transmission events (MacLean et al., 2021).”
InfluentialSelf-citationCoulombe, B. (2020) · Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature · doi:10.3410/f.738979608.793580713 · Cited by 201
A SARS-CoV-2 vaccine candidate would likely match all currently circulating variants
Dearlove, B. L., Lewitus, É., Bai, H., Li, Y., Reeves, D. B., Joyce, M. G., Scott, P. T., Amare, M. F., Vasan, S., Michael, N. L., et al. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2008281117 · Cited by 199 · cited 1× · see citing works
“Besides immune evasion, other plausible contributors to the fitness advantage of viruses in the 501Y lineages are: (1) that they produce more particles at anatomical sites suitable for optimal droplet or aerosol transmission, (2) that they produce particles that individually have physical properties that increase thei…”
BackgroundFurin Cleavage Site Is Key to SARS-CoV-2 PathogenesisPreprint
Johnson, B. A., Xie, X., Kalveram, B., Lokugamage, K. G., Muruato, A. E., Zou, J., Zhang, X., Juelich, T. L., Smith, J. K., Zhang, L., et al. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.08.26.268854 · Cited by 186 · see citing works
Self-citationKlassen, D. (1975) · ACM '75 · doi:10.1145/800181.810353 · Cited by 179
Nelson, G., Buzko, O. V., Spilman, P., Niazi, K., Rabizadeh, S., & Soon‐Shiong, P. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.01.13.426558 · Cited by 175 · cited 3× · see citing works
“Whereas in the presence of 501N, 484K has a modest positive impact on ACE2 binding (Starr et al., 2020), when present with 501Y, these mutations together synergistically increase ACE2-RBD binding affinity ~12.7 fold (Nelson et al., 2021; Zahradnik et al., 2021).”
InfluentialSimonsen, M., Mailund, T., & Pedersen, C. N. S. (2008) · Workshop on Algorithms in Bioinformatics · doi:10.1007/978-3-540-87361-7_10 · Cited by 174 · cited 1× · see citing works
“We next reconstructed phylogenetic trees for the remaining haplotype sequences using RapidNJ (Simonsen et al., 2008).”
SARS-CoV-2 one year on: evidence for ongoing viral adaptation
Peacock, T. P., Penrice-Randal, R., Hiscox, J. A., & Barclay, W. (2021) · Journal of General Virology · doi:10.1099/jgv.0.001584 · Cited by 149 · cited 3× · see citing works
“…RNA polymerase protein (Garvin et al., 2020), both of which may have increased viral transmissibility without impacting pathogenesis (reviewed in (Peacock et al., 2021)), few mutations were epidemiologically significant and the evolutionary dynamics of the virus were predominantly characterized…”
InfluentialPybus, O. G., Rambaut, A., Belshaw, R., Freckleton, R. P., Drummond, A. J., & Holmes, E. C. (2007) · Molecular Biology and Evolution · doi:10.1093/molbev/msm001 · Cited by 140 · see citing works
Interferon resistance of emerging SARS-CoV-2 variants
Guo, K., Barrett, B. S., Morrison, J. H., Mickens, K. L., Vladar, E. K., Hasenkrug, K. J., Poeschla, E. M., & Santiago, M. L. (2022) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2203760119 · Cited by 136 · see citing works
HIV-Specific Probabilistic Models of Protein Evolution
Nickle, D. C., Heath, L., Jensen, M. A., Gilbert, P. B., Mullins, J. I., & Pond, S. L. K. (2007) · PLoS ONE · doi:10.1371/journal.pone.0000503 · Cited by 125 · cited 1× · see citing works
“…in GISAID which have these errors), following which these translated sequences were mapped to the NCBI SARS-CoV-2 genome reference using the bealign tool from the BioExt package (github.com/veg/bioext) using the scoring matrix developed for rapidly evolving RNA viruses (Nickle et al., 2007).”
Nguyen, T. T., Pathirana, P. N., Nguyen, Q. V. H., Nguyen, Q. V. H., Bhatti, A., Nguyen, N. D., Nguyen, Q. V. H., Nguyen, N. D., Creighton, D., & Abdelrazek, M. (2021) · Scientific Reports · doi:10.1038/s41598-021-83105-3 · Cited by 109 · see citing works
An Evolutionary-Network Model Reveals Stratified Interactions in the V3 Loop of the HIV-1 Envelope
Poon, A. F. Y., Lewis, F. I., Pond, S. L. K., & Frost, S. D. W. (2007) · PLoS Computational Biology · doi:10.1371/journal.pcbi.0030231 · Cited by 106 · cited 2× · see citing works
“Second, analyses in such settings need to account for a well-known feature of viral evolution (Poon et al., 2007) where terminal branches include “dead-end” mutation events within individual hosts which, although maladaptive or deleterious at the population level (Pybus et al., 2007), have not been…”
Evolution of enhanced innate immune evasion by the SARS-CoV-2 B.1.1.7 UK variant
Thorne, L. G., Bouhaddou, M., Reuschl, A.-K., Zuliani-Alvarez, L., Polacco, B., Pelin, A., Batra, J., Whelan, M. V. X., Ummadi, M., Rojc, A., et al. (2021) · doi:10.1101/2021.06.06.446826 · Cited by 91 · see citing works
Nguyen, T. T., Pathirana, P., Nguyen, T., et al. (2020) · Scientific Reports · doi:10.1101/2020.07.10.171769 · Cited by 78 · cited 1×
“This amino acid change is predicted to have a modest impact on the structure of spike (Nguyen et al., 2021) and also protects from some neutralizing monoclonal antibodies (McCallum et al., 2021).”
Interferon Resistance of Emerging SARS-CoV-2 VariantsPreprint
Guo, K., Barrett, B. S., Mickens, K. L., Vladar, E. K., Morrison, J., Hasenkrug, K., Poeschla, E., & Santiago, M. L. (2021) · bioRxiv · doi:10.1101/2021.03.20.436257 · Cited by 77 · cited 2× · see citing works
“Relative to some of the earliest characterized SARS-CoV-2 A and B variants, V1 and V2 viruses have demonstrably less sensitivity to type I interferons (Guo et al., 2021; Thorne et al., 2021) and V1 displays greater antagonism of type I interferon mediated immune activation during the early stages of infection in cultu…”
Dudas, G., Hong, S. L., Potter, B., Calvignac-Spencer, S., Niatou-Singa, F. S., Tombolomako, T. B., Fuh-Neba, T., Vickos, U., Ulrich, M., Leendertz, F. H., et al. (2021) · doi:10.1101/2021.05.04.21256637 · Cited by 76 · cited 9× · see citing works
“Other prominent VOC, VOI and VUI lineages, however, had very few matches.”
InfluentialDudas, G., Hong, S. L., Potter, B. I., Calvignac‐Spencer, S., Niatou-Singa, F. S., Tombolomako, T. B., Neba, T. F., Vickos, U., Ulrich, M., Leendertz, F. H., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-26055-8 · Cited by 75 · see citing works
Lubinski, B., Fernandes, M. H. V., Frazier, L. E., et al. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.04.06.438731 · Cited by 71 · see citing works
Brown, J. C., Goldhill, D. H., Zhou, J., Peacock, T. P., Frise, R., Goonawardane, N., Baillon, L., Kugathasan, R., Pinto, A., McKay, P. F., et al. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.02.24.432576 · Cited by 68 · see citing works
Rapid detection of inter-clade recombination in SARS-CoV-2 with Bolotie
Varabyou, A., Pockrandt, C., Salzberg, S. L., & Pertea, M. (2021) · Genetics · doi:10.1093/genetics/iyab074 · Cited by 68 · see citing works
Garvin, M. R., Prates, E. T., Pavicic, M., Jones, P. C., Amos, B. K., Geiger, A., Shah, M. B., Streich, J., Gazolla, J. G. F. M., Kainer, D., et al. (2020) · Genome biology · doi:10.1186/s13059-020-02191-0 · Cited by 63 · cited 3× · see citing works
“There were, however, indications that some sites in the genome had experienced episodes of positive selection (Garvin et al., 2020; Korber et al., 2020; Plante et al., 2021; Zhang et al., 2020).”
Genomic Evidence of a Sars-Cov-2 Reinfection Case With E484K Spike Mutation in BrazilPreprint
Nonaka, C. K. V., Franco, M. M., Gräf, T., Mendes, A. V. A., Aguiar, R. S., Giovanetti, M., & Souza, B. S. D. F. (2021) · Preprints.org · doi:10.20944/preprints202101.0132.v1 · Cited by 60 · see citing works
Increased infections, but not viral burden, with a new SARS-CoV-2 variant
Walker, A. S., Vihta, K.-D., Gethings, O., Pritchard, E., Jones, J., House, T., Bell, I., Bell, J. I., Newton, J. N., Farrar, J., et al. (2021) · doi:10.1101/2021.01.13.21249721 · Cited by 58 · see citing works
Tablizo, F. A., Kim, K. M., Lapid, C. M., Castro, M. J. R., Yangzon, M. S. L., Maralit, B. A., Ayes, M. E. C., Cutiongco-de la Paz, E. M., De Guzman, A. R., Yap, J. M. C., et al. (2021) · doi:10.1101/2021.03.03.21252812 · Cited by 46 · cited 2× · see citing works
“Additionally, whereas a convergent A701V mutation is also found in the B.1.526 and S/E484K carrying lineage that was first identified in New York (Annavajhala et al., 2021), P681H is found in the S/E484K and S/N501Y carrying P.3 lineage first identified in the Philippines (Tablizo et al., 2021), and both S/H655Y and S…”
InfluentialPrioritization of SARS-CoV-2 epitopes using a pan-HLA and global population inference approachPreprint
Campbell, K. M., Steiner, G., Wells, D. K., Ribas, A., & Kalbasi, A. K. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.03.30.016931 · Cited by 46 · cited 1× · see citing works
“The precise biological significance of the L5F mutation remains unknown but it falls within CTL epitopes that are predicted to be recognizable by a broad array of different HLA types (Campbell et al., 2020) and is therefore potentially a CTL escape mutation.”
BackgroundSARS-CoV-2 is well adapted for humans. What does this mean for re-emergence?Preprint
Zhan, S. H., Deverman, B. E., & Chan, Y. A. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.05.01.073262 · Cited by 35 · see citing works
Du, W., Wolfert, M., Peeters, B., et al. (2020) · PLoS Pathogens · doi:10.1371/journal.ppat.1008816 · Cited by 34
MacLean, O. A., Lytras, S., Weaver, S., Singer, J. B., Boni, M. F., Lemey, P., Pond, S. L. K., & Robertson, D. L. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.05.28.122366 · Cited by 33 · cited 1× · see citing works
“Besides immune evasion, other plausible contributors to the fitness advantage of viruses in the 501Y lineages are: (1) that they produce more particles at anatomical sites suitable for optimal droplet or aerosol transmission, (2) that they produce particles that individually have physical properties that increase thei…”
Self-citationLubinski, B., Fernandes, M. H. V., Frazier, L. E., Tang, T., Daniel, S., Diel, D. G., Jaimes, J. A., & Whittaker, G. R. (2021) · SSRN Electronic Journal · doi:10.2139/ssrn.3889709 · Cited by 31 · cited 3× · see citing works
“…(Johnson et al., 2021; Lau et al., 2020) and the P681H mutation - which falls within this site - likely increases the efficiency of furin cleavage by replacing a less favourable uncharged amino acid with a more favourable positively charged basic one (Garry et al., 2021; Lubinski et al., 2021).”
Althaus, C. L., Baggio, S., Reichmuth, M. L., Hodcroft, E. B., Riou, J., Neher, R. A., Jacquérioz, F., Spechbach, H., Salamun, J., Vetter, P., et al. (2021) · medRxiv · doi:10.1101/2021.06.10.21258468 · Cited by 30 · cited 1× · see citing works
“…receptor affinity (V1, V2 and V3) (Nelson et al., 2021; Starr et al., 2020; Zahradnik et al., 2021), increased transmissibility (V1, V2 and V3) (Althaus et al., 2021; Faria et al., 2021; Lubinski et al., 2021; Pearson et al., 2021; Public Health England, 2020; Volz et al., 2021), substantially…”
Self-citationde Oliveira, T., Lutucuta, S., Nkengasong, J. N., Morais, J. F. M., Paixão, J., Neto, Z., Afonso, P., Miranda, J., David, K., Inglês, L., et al. (2021) · medRxiv · doi:10.1101/2021.03.30.21254323 · Cited by 28 · cited 1× · see citing works
“V2 lineage first identified in Tanzanian travellers (de Oliveira et al., 2021).”
Self-citationIn vitro evolution of Remdesivir resistance reveals genome plasticity of SARS-CoV-2
Szemiel, A., Merits, A., Orton, R., et al. (2021) · bioRxiv · doi:10.1101/2021.02.01.429199 · Cited by 15
Self-citationEvidence of significant natural selection in the evolution of SARS-CoV-2 in bats, not humans
(2020) · TUScholarShare (Temple University) · doi:10.34944/dspace/225 · Cited by 14 · see citing works
RASCL: 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 · see citing works
Self-citationRhee, S., Magalis, B., Hurley, L., et al. (2019) · Open Forum Infectious Diseases · doi:10.1093/ofid/ofz135 · Cited by 9 · see citing works
Abstract S03-01: Pan-HLA prediction of SARS-CoV-2 epitopes
Campbell, K. M., Steiner, G., Wells, D. K., et al. (2020) · Clinical Cancer Research · doi:10.1158/1557-3265.covid-19-s03-01 · Cited by 2 · cited 1× · see citing works
“S/18 falls within multiple different predicted CTL epitopes (Campbell et al., 2020) and the L18F mutation is known to reduce viral sensitivity to some neutralizing monoclonal antibodies (McCallum et al., 2021).”
Emergence and Expansion of the SARS-CoV-2 Variant B.1.526 Identified in New York
Annavajhala, M. K., Mohri, H., Wang, P., Nair, M., Zucker, J. E., Sheng, Z., Gomez-Simmonds, A., Kelley, A. L., Tagliavia, M., Huang, Y., et al. (2021) · doi:10.1101/2021.02.23.21252259 · cited 7×
“The lineages containing sequences with the most matches were B.1.526 and B.1.621 (both with modal matches = 5 and maximum = 7), suggesting that they too are possibly scaling the same fitness peak as the 501Y lineage viruses.”
Influential
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Research works printed but not linked: 2
- Campbell, K.M., Steiner, G., Wells, D.K., Ribas, A., and Kalbasi, A. (2020). Prediction of SARS-CoV-2 epitopes across 9360 HLA class I alleles. BioRxiv.
- Pearson, C.A., Russell, T.W., Davies, N., and Kucharski, A.J. (2021). Estimates of severity and transmissibility of novel SARS-CoV-2 variant 501Y.V2 in South Africa | CMMID Repository.
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SARS-CoV-2 variants, spike mutations and immune escape
Harvey, W. T., Carabelli, A. M., Jackson, B., Gupta, R. K., Thomson, E. C., Harrison, E. M., Ludden, C., Reeve, R., Rambaut, A., COVID-19 Genomics UK (COG-UK) Consortium, et al. (2021) · Nature Reviews Microbiology · doi:10.1038/s41579-021-00573-0 · Cited by 3,528 · see citing works
Self-citationThe biological and clinical significance of emerging SARS-CoV-2 variants
Tao, K., Tzou, P. L., Nouhin, J., Gupta, R. K., de Oliveira, T., Kosakovsky Pond, S. L., Fera, D., & Shafer, R. W. (2021) · Nature Reviews Genetics · doi:10.1038/s41576-021-00408-x · Cited by 1,009 · see citing works
Self-citationThe emergence, genomic diversity and global spread of SARS-CoV-2
Li, J., Lai, S., Gao, G. F., & Shi, W. (2021) · Nature · doi:10.1038/s41586-021-04188-6 · Cited by 408 · see citing works
COVID-19 in Amazonas, Brazil, was driven by the persistence of endemic lineages and P.1 emergence
Naveca, F. G., do Nascimento, V. A., de Souza, V. C., Corado, A. D. L. G., Nascimento, F., Silva, G., Costa, Á., Duarte, D., Pessoa, K., Mejía, M., et al. (2021) · Nature Medicine · doi:10.1038/s41591-021-01378-7 · Cited by 475 · see citing works
Predicting the mutational drivers of future SARS-CoV-2 variants of concern
Maher, M. C., Bartha, I., Weaver, S., di Iulio, J., Ferri, E., Soriaga, L. B., Lempp, F. A., Hie, B., Bryson, B. D., Berger, B., et al. (2022) · Science Translational Medicine · doi:10.1126/scitranslmed.abk3445 · Cited by 178 · see citing works
Self-citationFocosi, D., & Maggi, F. (2021) · Reviews in Medical Virology · doi:10.1002/rmv.2231 · Cited by 148 · see citing works
Early detection and surveillance of SARS-CoV-2 genomic variants in wastewater using COJAC
Jahn, K., Dreifuss, D., Topolsky, I., Kull, A., Ganesanandamoorthy, P., Fernández-Cassi, X., Bänziger, C., Devaux, A. J., Stachler, E. N., Caduff, L., et al. (2022) · Nature Microbiology · doi:10.1038/s41564-022-01185-x · Cited by 212 · see citing works
Detection and characterization of the SARS-CoV-2 lineage B.1.526 in New York
West, A. P., Wertheim, J. O., Wang, J. C., Vasylyeva, T. I., Havens, J. L., Chowdhury, M. A., Gonzalez, E., Fang, C. E., Lonardo, S. S. D., Hughes, S., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-25168-4 · Cited by 130 · see citing works
Self-citationAngiotensin-converting enzyme 2—at the heart of the COVID-19 pandemic
Oudit, G. Y., Wang, K., Viveiros, A., Kellner, M. J., & Penninger, J. M. (2023) · Cell · doi:10.1016/j.cell.2023.01.039 · Cited by 131 · see citing works
A look into the future of the COVID-19 pandemic in Europe: an expert consultation
Iftekhar, E. N., Priesemann, V., Balling, R., Bauer, S., Beutels, P., Valdez, A. C., Cuschieri, S., Czypionka, T., Dumpis, U., Glaab, E., et al. (2021) · The Lancet Regional Health - Europe · doi:10.1016/j.lanepe.2021.100185 · Cited by 127 · see citing works
The impact of viral mutations on recognition by SARS-CoV-2 specific T cells
de Silva, T. I., Liu, G., Lindsey, B. B., Dong, D., Moore, S. C., Hsu, S. N., Shah, D. R., Wellington, D., Mentzer, A. J., Angyal, A., et al. (2021) · iScience · doi:10.1016/j.isci.2021.103353 · Cited by 89 · see citing works
Signatures in SARS-CoV-2 spike protein conferring escape to neutralizing antibodies
Alenquer, M., Ferreira, F., Lousa, D., Valério, M., Medina-Lopes, M., Bergman, M., Gonçalves, J., Demengeot, J., Leite, R. B., Lilue, J., et al. (2021) · PLoS Pathogens · doi:10.1371/journal.ppat.1009772 · Cited by 99 · see citing works
SARS-CoV-2 variants and COVID-19 vaccines: Current challenges and future strategies
Gong, W., Parkkila, S., Wu, X., & Aspatwar, A. (2022) · International Reviews of Immunology · doi:10.1080/08830185.2022.2079642 · Cited by 74 · see citing works
“These findings suggested that reduction in immunity is evident after the immunization with current vaccines and may necessitate several booster shots to protect against future infections with SARS-CoV-2 [101].”
BackgroundContributions of adaptation and purifying selection to SARS-CoV-2 evolution
Neher, R. A. (2022) · Virus Evolution · doi:10.1093/ve/veac113 · Cited by 56 · see citing works
One year into the pandemic: Short-term evolution of SARS-CoV-2 and emergence of new lineages
Gónzález‐Candelas, F., Shaw, M., Phan, T. G., Kulkarni‐Kale, U., Paraskevis, D. N., Luciani, F., Kimura, H., & Sironi, M. (2021) · Infection Genetics and Evolution · doi:10.1016/j.meegid.2021.104869 · Cited by 65 · see citing works
Peterson, S. W., Lidder, R., Daigle, J., Wonitowy, Q., Dueck, C., Nagasawa, A., Mulvey, M. R., & Mangat, C. S. (2021) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2021.151283 · Cited by 52 · see citing works
Kumar, S., Tao, Q.-Q., Weaver, S., et al. (2020) · bioRxiv · doi:10.1101/2020.09.24.311845 · Cited by 55
Self-citationResende, P. C., Naveca, F. G., Lins, R. D., Dezordi, F. Z., Ferraz, M. V. F., Moreira, E. G., Coêlho, D. F., Motta, F. C., Paixão, A. C. D., Appolinario, L., et al. (2021) · Virus Evolution · doi:10.1093/ve/veab069 · Cited by 46 · see citing works
Resende, P. C., Gräf, T., Paixão, A. C. D., Appolinario, L., Lopes, R. S., Mendonça, A. C. D. F., da Rocha, A. S. B., Motta, F. C., Neto, L. G. L., Khouri, R., et al. (2021) · Viruses · doi:10.3390/v13050724 · Cited by 43 · see citing works
“2 in late-July 6 and shortly precede the detection of a major global shift in the SARS-CoV-2 fitness landscape after October 2020 [20].”
BackgroundSARS‐CoV‐2 virulence evolution: Avirulence theory, immunity and trade‐offs
Alizon, S., & Sofonea, M. T. (2021) · Journal of Evolutionary Biology · doi:10.1111/jeb.13896 · Cited by 46 · see citing works
“M ut at io ns o f c on ce rn a re h ig hl ig ht ed in it al ic . and E484K mutations found in, respectively, all three and two previous VOCs illustrates the limits of SARS- CoV- 2 convergent evolution (Martin et al., 2021) and challenges the current existence of strong genomic bottlenecks.”
BackgroundResultInfluentialKmieć, D., Lista, M. J., Ficarelli, M., Swanson, C. M., & Neil, S. J. D. (2021) · PLoS Pathogens · doi:10.1371/journal.ppat.1009726 · Cited by 43 · see citing works
Scheepers, C., Everatt, J., Amoako, D., et al. (2021) · medRxiv · doi:10.1101/2021.08.20.21262342 · Cited by 43 · see citing works
Self-citationLam, C., Gray, K.-A., Gall, M. L., Sadsad, R., Arnott, A., Johnson-Mackinnon, J. C., Fong, W., Basile, K., Kok, J., Dwyer, D. E., et al. (2021) · Journal of Clinical Microbiology · doi:10.1128/jcm.01046-21 · Cited by 46 · see citing works
Lamarca, A. P., de Almeida, L. G. P., Francisco, R. D. S., Agnez‐Lima, L. F., Scortecci, K. C., Perez, V. P., Brustolini, O. J. B., Sousa, E. S. S., Secco, D., Santos, Â., et al. (2021) · PLoS neglected tropical diseases · doi:10.1371/journal.pntd.0009835 · Cited by 33 · see citing works
COVID-19, the first pandemic in the post-genomic era
van Dorp, L., Houldcroft, C. J., Richard, D., & Balloux, F. (2021) · Current Opinion in Virology · doi:10.1016/j.coviro.2021.07.002 · Cited by 46 · see citing works
“Finally, selection screens based on patterns of non-synonymous and synonymous mutations [51] and homoplasy-based metrics [25] may hold scope to predict the adaptive potential of a variant based on its constituent mutations.”
BackgroundGarushyants, S. K., Rogozin, I. B., & Koonin, E. V. (2021) · Communications Biology · doi:10.1038/s42003-021-02858-9 · Cited by 45 · see citing works
Yang, Z. L., Zhang, S., Tang, Y., Zhang, S., Xu, D.-Q., Yue, S., & Liu, Q. (2022) · Aging and Disease · doi:10.14336/ad.2021.1210 · Cited by 44 · see citing works
Epidemiological dynamics of SARS-CoV-2 VOC Gamma in Rio de Janeiro, Brazil
Moreira, F. R. R., D’arc, M., Mariani, D., Herlinger, A. L., Schiffler, F. B., Rossi, Á. D., Leitão, I. D. C., Miranda, T. D. S., Cosentino, M. A. C., Tôrres, M. C. D. P., et al. (2021) · Virus Evolution · doi:10.1093/ve/veab087 · Cited by 34 · see citing works
“This observation highlights the previously reported evolutionary convergence on SARS-CoV-2 genomes (Martin et al., 2021).”
BackgroundIron dysregulation in COVID‐19 and reciprocal evolution of SARS‐CoV‐2: Natura nihil frustra facit
Gupta, Y., Maciorowski, D., Medernach, B., Becker, D. P., Durvasula, R., Libertin, C. R., & Kempaiah, P. M. (2022) · Journal of Cellular Biochemistry · doi:10.1002/jcb.30207 · Cited by 32 · see citing works
Gräf, T., Bello, G., Venas, T. M. M., Pereira, E. C., Paixão, A. C. D., Appolinario, L., Lopes, R. S., Mendonça, A. C. D. F., da Rocha, A. S. B., Motta, F. C., et al. (2021) · Virus Evolution · doi:10.1093/ve/veab091 · Cited by 33 · see citing works
Challenges in modeling the emergence of novel pathogens
Glennon, E. E., Bruijning, M., Lessler, J., Miller, I. F., Rice, B. L., Thompson, R. N., Wells, K., & Metcalf, C. J. E. (2021) · Epidemics · doi:10.1016/j.epidem.2021.100516 · Cited by 36 · see citing works
“For SARS-CoV-2, in early 2021, variants of concern feature plasticity in combinations of traits encompassing receptor avidity, immune escape, transmissibility and virulence (Martin et al., 2021).”
BackgroundKumar, S., Tao, Q., Weaver, S., Sanderford, M. D., Caraballo‐Ortiz, M. A., Sharma, S., Pond, S. L. K., & Miura, S. (2021) · Molecular Biology and Evolution · doi:10.1093/molbev/msab118 · Cited by 68 · see citing works
Self-citationRadu, E. L., Masseron, A., Amman, F., Schedl, A., Agerer, B., Endler, L., Penz, T., Bock, C., Bergthaler, A., Vierheilig, J., et al. (2022) · Water Research · doi:10.1016/j.watres.2022.118257 · Cited by 25 · see citing works
“…of more contagious variants (Variants of Concern – VOCs and Variants of Interest - VOIs), sequencing techniques proved to be the most valuable strategy to provide a deep and accurate understanding of the new circulating lineages (Fontenele et al., 2021; Martin et al., 2020; Rambaut et al., 2020b).”
Beta RBD boost broadens antibody-mediated protection against SARS-CoV-2 variants in animal models
Sheward, D. J., Mandolesi, M., Urgard, E., Kim, C., Hanke, L., Vidakovics, L. P., Pankow, A. P., Smith, N. L., Dopico, X. C., McInerney, G. M., et al. (2021) · Cell Reports Medicine · doi:10.1016/j.xcrm.2021.100450 · Cited by 27 · see citing works
Self-citationMutyambizi, C., Dunlop, J., Maluleke, C., et al. (2021) · South African medical journal = Suid-Afrikaanse tydskrif vir geneeskunde · doi:10.7196/samj.2021.v111i12.15822 · Cited by 22
“The daily cases then declined before a major surge in December, when the country experienced its second wave of increased cases, probably fuelled by a new variant of the virus.[4] Like many other countries globally, SA implemented an unprecedented national shutdown to combat the spread of the virus.”
BackgroundDecomposing the sources of SARS-CoV-2 fitness variation in the United States
Kepler, L. M., Hamins-Puértolas, M., & Rasmussen, D. A. (2021) · Virus Evolution · doi:10.1093/ve/veab073 · Cited by 24 · see citing works
“…multiple lineages have independently acquired amino acid mutations suspected to increase transmission potential or escape immunity, including Spike E484K, Spike N501Y and Spike Q677P/H (Hodcroft et al., 2021; Martin et al., 2021), suggesting that lineages are adapting through convergent evolution.”
BackgroundMolecular beacons allow specific RT-LAMP detection of B.1.1.7 variant SARS-CoV-2
Sherrill-Mix, S., Duyne, G. V. V., & Bushman, F. (2021) · medRxiv · doi:10.1101/2021.03.25.21254356 · Cited by 21
Richard, D., Shaw, L. P., Lanfear, R., Corbett-Detig, R. B., Hinrichs, A. S., McBroome, J., Turakhia, Y., Acman, M., Owen, C. J., Tan, C. C. S., et al. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.05.06.442903 · Cited by 20 · see citing works
“We can now rearrange this expression for δ P T # · (12)”
BackgroundMallm, J., Bundschuh, C., Kim, H., Weidner, N., Steiger, S., Lander, I., Börner, K., Bauer, K., Hübschmann, D., Beneš, V., et al. (2021) · medRxiv · doi:10.1101/2021.04.27.21254849 · Cited by 16 · see citing works
“Variants of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), the virus causing coronavirus disease 2019 ( Covid-19 Covid-19 ), are of concern with respect Mutation N501Y has been found to render the virus more infectious, most likely by increasing affinity for the ACE2-receptor (14-17).”
Yaseen, A. R., Suleman, M., Qadri, A. S., Ali, A., Arshad, I., & Khan, D. M. (2023) · In Silico Pharmacology · doi:10.1007/s40203-023-00156-2 · Cited by 22 · see citing works
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 18 · see citing works
Franceschi, V. B., Ferrareze, P. A. G., Zimerman, R. A., Cybis, G. B., & Thompson, C. E. (2021) · Virus Research · doi:10.1016/j.virusres.2021.198532 · Cited by 25 · see citing works
Buchan, S., Tibebu, S., Daneman, N., et al. (2021) · medRxiv · doi:10.1101/2021.03.31.21254502 · Cited by 16
Alisoltani, A., Jaroszewski, L., Iyer, M., Iranzadeh, A., & Godzik, A. (2022) · Frontiers in Genetics · doi:10.3389/fgene.2022.875406 · Cited by 19 · see citing works
“Signatures of positive selection for NSP6 Δ106-108 were recently reported (Martin et al., 2021) in line with our results showing high recurrence of NSP6 deletions (Figure 4B).”
ResultFranceschi, V. B., Caldana, G. D., Perin, C., Horn, A., Peter, C., Cybis, G. B., Ferrareze, P. A. G., Rotta, L. N., Cadegiani, F., Zimerman, R. A., et al. (2021) · Pathogens · doi:10.3390/pathogens10080988 · Cited by 13 · see citing works
Phylogenomic Evidence of Reinfection and Persistence of SARS-CoV-2: First Report from Colombia
Ramírez, J. D., Muñoz, M., Ballesteros, N., Patiño, L. H., Castañeda, S., Rincón, C. A., Méndez, C., Oliveros, C., Perez, J., Márquez, E. K., et al. (2021) · Vaccines · doi:10.3390/vaccines9030282 · Cited by 17 · see citing works
Conformational stability of SARS-CoV-2 glycoprotein spike variants
Arruda, H. R. S., Lima, T. M., Alvim, R. G. F., Victorio, F. B. A., de Abreu, D. P. B., Marsili, F. F., Cruz, K. D., Marques, M. A., Sosa‐Acosta, P., Quiñones‐Vega, M., et al. (2022) · iScience · doi:10.1016/j.isci.2022.105696 · Cited by 13 · see citing works
The seasonal behaviour of COVID-19 and its galectin-like culprit of the viral spike
Caetano-Anollés, K., Hernandez, N., Mughal, F., Tomaszewski, T., & Caetano‐Anollés, G. (2022) · Methods in microbiology · doi:10.1016/bs.mim.2021.10.002 · Cited by 14 · see citing works
“Similarly, the rise of VOCs appears to coincide with a major global shift in the selective landscape that involves convergence between lineages (Martin et al., 2021).”
BackgroundNunes, D. R., Braconi, C. T., Ludwig‐Begall, L. F., Arns, C. W., & Durães‐Carvalho, R. (2022) · PLoS ONE · doi:10.1371/journal.pone.0268389 · Cited by 13 · see citing works
Castelán-Sánchez, H., Delaye, L., Inward, R., et al. (2023) · bioRxiv · doi:10.1101/2022.07.05.498834 · Cited by 9 · see citing works
SARS-CoV-2 mutational cascades and the risk of hyper-exponential growth
Halley, J. M., Vokou, D., Παππάς, Γ., & Sainis, I. (2021) · Microbial Pathogenesis · doi:10.1016/j.micpath.2021.105237 · Cited by 13 · see citing works
Jumping a Moving Train: SARS-CoV-2 Evolution in Real Time
Moustafa, A. M., & Planet, P. J. (2021) · Journal of the Pediatric Infectious Diseases Society · doi:10.1093/jpids/piab051 · Cited by 8 · see citing works
Chen, P. E., & Shapiro, B. (2021) · bioRxiv · doi:10.1101/2021.06.30.450606 · Cited by 9
“Intriguingly, many of the variants of concern (VOCs) identified thus far harbor mutations (e.g., E484K in the spike gene) that are thought to be under convergent selection [33].”
BackgroundLeung, L. Y. T., Khan, S., Budylowski, P., Li, Z.-J., Goroshko, S., Liu, Y., Dong, S., Carlyle, J., Rini, J., Ostrowski, M., et al. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.659071 · Cited by 10 · see citing works
Alenquer, M., Ferreira, F., Lousa, D., Valério, M., Medina-Lopes, M., Bergman, M., Gonçalves, J., Demengeot, J., Leite, R. B., Lilue, J., et al. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.04.22.441007 · Cited by 8 · see citing works
Dynamics of natural selection preceding human viral epidemics and pandemics
Havens, J. L., Pond, S. L. K., Zehr, J. D., et al. (2025) · bioRxiv · doi:10.1101/2025.02.26.640439 · Cited by 7
“SARS-CoV-2 accumulated advantageous mutations within the first year of widespread circulation, including D614G which increased transmissibility 18,19 and N501Y, which together with a cluster of other mutations that arose in multiple variants of concern 20 , increased receptor binding efficiency..”
Self-citationColson, P., Delerce, J., Burel, E., Beye, M., Fournier, P., Levasseur, A., Lagier, J., & Raoult, D. (2021) · Virus Genes · doi:10.1007/s11262-021-01877-2 · Cited by 8 · see citing works
Riou, C., Keeton, R., Moyo-Gwete, T., et al. (2021) · medRxiv · doi:10.1101/2021.06.03.21258307 · Cited by 7
Self-citationSARS-CoV-2 convergent evolution as a guide to explore adaptive advantagePreprint
Zahradník, J., Nunvář, J., & Schreiber, G. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.05.24.445534 · Cited by 6 · see citing works
Garushyants, S. K., Rogozin, I. B., & Koonin, E. V. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.04.23.441209 · Cited by 7 · see citing works
Rowe, L. A., Beddingfield, B. J., Goff, K. A., Killeen, S. Z., Chirichella, N. R., Melton, A., Roy, C. J., & Maness, N. J. (2022) · Viruses · doi:10.3390/v14010077 · Cited by 6 · see citing works
Accurate Detection of Convergent Mutations in Large Protein Alignments With ConDor
Morel, M. H., Zhukova, A., Lemoine, F., & Gascuel, O. (2024) · Genome Biology and Evolution · doi:10.1093/gbe/evae040 · Cited by 7 · see citing works
“…where one first identified mutations in the Spike protein, which were spreading within the viral population and appeared multiple times independently, before being demonstrated to be evolutionarily advantageous for the virus (van Dorp et al. 2020; Korber et al. 2020; Martin et al. 2021).”
BackgroundSARS-CoV-2’s evolutionary capacity is mostly driven by host antiviral moleculesPreprint
Lamb, K. D., Luka, M. M., Saathoff, M., Orton, R. J., Phan, M. V. T., Cotten, M. L., Yuan, K., & Robertson, D. L. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.04.07.536037 · Cited by 4 · see citing works
“Contrary to geographical variation in emergence of SARS-CoV-2 variants [11–14], we also witness commonality of mutations across independent variants[15], indicating convergent evolution[16].”
Self-citationContrasting Patterns in the Early Stage of SARS-CoV-2 Evolution between Humans and Minks
Tai, J., Sun, H.-Y., Tseng, Y.-C., Li, G., Chang, S., Yeh, S., Chen, P., Chaw, S., & Wang, H. (2022) · Molecular Biology and Evolution · doi:10.1093/molbev/msac156 · Cited by 3 · see citing works
Ferrareze, P. A. G., Zimerman, R. A., Franceschi, V. B., Caldana, G. D., Netz, P. A., & Thompson, C. E. (2022) · Journal of Biomolecular Structure and Dynamics · doi:10.1080/07391102.2022.2076154 · Cited by 4 · see citing works
“coevolutionary mutational processes (Martin et al., 2021).”
BackgroundLimited spread of a rare spike E484K-harboring SARS-CoV-2 in Marseille, France
Colson, P., Fantini, J., Yahi, N., Delerce, J., Levasseur, A., Fournier, P., Lagier, J., Raoult, D., & Scola, B. L. (2022) · Archives of Virology · doi:10.1007/s00705-021-05331-4 · Cited by 4 · see citing works
Rapid expansion of SARS-CoV-2 variants of concern is a result of adaptive epistasisPreprint
Garvin, M. R., Prates, E. T., Romero, J., Cliff, A., Gazolla, J. G. F. M., Pickholz, M., Pavicic, M., & Jacobson, D. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.08.03.454981 · Cited by 10 · see citing works
“…those in S (Asn501Tyr, Ser477Asn, and Pro681His) are the result of multiple independent mutation events because they are under positive selection (Martin et al. 2021), but we also identified a mutation in nsp3 that is one of the lineage-defining mutations for B.1.1.7 and appears in disjoint…”
BackgroundInfluentialVariations from SARS-CoV-2 to Omicron: A new threat knocking at world's door
Balkrishna, A., Rohela, A., Kumar, A., Arya, A., & Khan, N. (2022) · Journal of Applied Pharmaceutical Science · doi:10.7324/japs.2022.120404 · Cited by 3 · see citing works
Hernandez, M., Banu, R., Gonzalez-Reiche, A., Gray, B., Shrestha, P., Cao, L., Chen, F., Shi, H.-Z., Hanna, A., Ramírez, J., et al. (2021) · medRxiv · doi:10.1016/j.jmoldx.2022.04.003 · Cited by 2 · see citing works
Ferrareze, P. A. G., Zimerman, R., Franceschi, V. B., et al. (2021) · bioRxiv · doi:10.1101/2021.07.16.452571 · Cited by 2
“The presence of these sets of consistently present substitutions are highly suggestive of coevolutionary mutational processes (Martin et al., 2021).”
BackgroundAlisoltani, A., Jaroszewski, L., Iyer, M., Iranzadeh, A., & Godzik, A. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.07.04.451027 · Cited by 2 · see citing works
Driving potent neutralization of a SARS-CoV-2 Variant of Concern with a heterotypic boostPreprint
Sheward, D. J., Mandolesi, M., Urgard, E., Kim, C., Hanke, L., Vidakovics, L. P., Pankow, A. P., Smith, N. L., Dopico, X. C., McInerney, G. M., et al. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.04.03.438330 · Cited by 1 · see citing works
Self-citationEvolving SARS-CoV-2 variants and mutational cascades
Halley, J., Vokou, D., Pappas, G., et al. (2021) · medRxiv · doi:10.1101/2021.04.03.21254871 · Cited by 2
Long-range linkage effects in adapting sexual populations
Rouzine, I. M. (2023) · Scientific Reports · doi:10.1038/s41598-023-39392-z · Cited by 3 · see citing works
N’Guessan, A., Kailasam, S., Mostefai, F., Poujol, R., Grenier, J., Contini, P., Palma, R. D., Haber, C., Stadler, V., Bourque, G., et al. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.06.01.494373 · Cited by 1 · see citing works
SARS-CoV-2 convergent evolution cannot be reliably inferred from phylogenetic analysesPreprint
Jo, Y.-S., Tamuri, A. U., Towers, G. J., & Goldstein, R. A. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.05.15.444301
“This was surprising, because recurrent VOC mutations are widely believed to be homoplasic (Ferrareze et al., 2021; Lemmermann et al., 2021; Martin et al., 2021; Resende et al., 2021).”
BackgroundLombardi, L. P., Yang, H. M., Spira, B., et al. (2023) · Trends in Computational and Applied Mathematics · doi:10.5540/tcam.2023.024.04.00595
“The gamma variant harbours a total of 25 mutations (synonymous and non-synonymous) compared with its most closely related ancestral, including 10 amino acid substitutions in the spike protein, some of them associated with a higher degree of transmissibility [10] [11].”
Chen, D., Randhawa, G. S., Soltysiak, M. P. M., de Souza, C. P., Lila Kari, A., Singh, S. M., & Hill, K. A. (2022) · JMIR Bioinformatics and Biotechnology · doi:10.2196/42243
Uncovering the structural flexibility of SARS-CoV-2 glycoprotein spike variantsPreprint
Arruda, H. R. S., Lima, T. M., Alvim, R. G. F., Victorio, F. B. A., de Abreu, D. P. B., Marsili, F. F., Cruz, K. D., Sosa‐Acosta, P., Quiñones‐Vega, M., Guedes, J. D. S., et al. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.04.20.488873
Tai, J., Chaw, S., Sun, H.-Y., Tseng, Y.-C., Li, G., Chang, S., Yeh, S., Chen, P., & Wang, H. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.09.15.459215
“Assuming the SARS-CoV-2 population has grown exponentially [16, 19], the observed SFSs significantly deviated from neutral expectation under this population growth model [25] (Materials and Methods), further supporting the idea”
BackgroundResultInfluentialSARS-CoV-2 Variants and Clinical Implications: A Review Article
Zaputra, D., & Utama, I. M. S. (2024) · International Journal Of Scientific Advances · doi:10.51542/ijscia.v5i2.9
“[10] This finding was based on the failure to identify the S gene during examination using the PCR method. due to a deletion that is almost similar to the deletion found in the Alpha variant.”
BackgroundMethodInfluential
- Authors
- Martin, D. P., Weaver, S., Tegally, H., San, E. J., Shank, S. D., Wilkinson, E., Lucaci, A. G., Giandhari, J., Naidoo, S., Pillay, Y., Singh, L., Lessells, R. J., NGS-SA, (COG-UK), C.-1. G. U., Gupta, R. K., Wertheim, J. O., Nekturenko, A., Murrell, B., Harkins, G. W., Lemey, P., MacLean, O. A., Robertson, D. L., de Oliveira, T., & Kosakovsky Pond, S. L.
- Affiliations
- University of Cape Town (ZA)
- Temple University (US)
- University of KwaZulu-Natal (ZA)
- University of Cambridge (GB)
- University of California San Diego (US)
- Pennsylvania State University (US)
- Karolinska Institutet (SE)
- South African Medical Research Council (ZA)
- Rega Institute for Medical Research (BE)
- University of Washington (US)
- MRC University of Glasgow Centre for Virus Research (GB)
- Corresponding author
- Martin, Darren P
- ORCID
- Venue
- Cell
- Publisher
- openRxiv
- Published
- 2021-03-05
- Volume
- 184
- Issue
- 20
- Pages
- 5189-5200.e7
- ISSN
- 0092-8674 (ISSN-L)
- PMC
- PMC8421097
- OpenAlex
- W3198909684
- Cited by
- 291
- References
- 90
- Citations by year
- 2026: 14 · 2025: 12 · 2024: 30 · 2023: 58 · 2022: 100 · 2021: 66 · 2018: 1 · 2017: 1 · 2015: 1 · 2014: 2 · 2013: 1
- FWCI
- 20.11
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Cell (publishedVersion)
- medRxiv (acceptedVersion, cc-by-nd)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- ENLIGHTEN (Jurnal Bimbingan dan Konseling Islam) (submittedVersion, cc-by-sa)
- Lirias (submittedVersion)
- UWC Research Repository (University of the Western Cape) (submittedVersion)
- Apollo (University of Cambridge) (submittedVersion)
- Apollo
- Funders
- National Science Foundation (2027196)
- Gilead Sciences
- Wellcome Trust (U24HG006941, 725422, 108082/A/15/Z, 206369/Z/17/Z, Z/17/Z, 206298/Z/17/Z, 220977/Z/20/Z, 222574, 220977, 725422-ReservoirDOCS, 206369, 222574/Z/21/Z)
- UK Research and Innovation (MC_PC_19027)
- South African Medical Research Council
- National Institutes of Health (1U01Al152151-01, 5u01ai152151-05, H3ABioNet, AI140970)
- Centers for Disease Control and Prevention
- Medical Research Council (MC UU 12014/12, MC_PC_19026)
- National Human Genome Research Institute (U24HG006941)
- National Institute of Allergy and Infectious Diseases (U01 AI152151, R01AI140970, R01AI135992, R01AI134384)
- Topics
- Health Sciences › Medicine › Infectious Diseases › SARS-CoV-2 and COVID-19 Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
- Life Sciences › Agricultural and Biological Sciences › Animal Science and Zoology › Animal Virus Infections Studies
- Keywords
- SARS-CoV-2, Alpha variant, Beta variant, P.1 lineage, convergent evolution, adaptive evolution, host immune evasion, viral evolution, herd immunity
- MeSH terms
- COVID-19, SARS-CoV-2, Host Adaptation, Amino Acid Sequence, Codon, Genes, Viral, Humans, Mutation, Phylogeny, Public Health, Evolution, Molecular, Genetic Drift, Immune Evasion, Pandemics
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