The emergence and ongoing convergent evolution of the SARS-CoV-2 N501Y lineages

NGS-SA; The COVID-19 Genomics UK (COG-UK) Consortium; Darren P. Martin; Steven Weaver; Houriiyah Tegally; James Emmanuel San; Stephen D. Shank; Eduan Wilkinson; Alexander G. Lucaci; Jennifer Giandhari; Sureshnee Naidoo; Yeshnee Pillay; Lavanya Singh; Richard J. Lessells; Ravindra K. Gupta; Joel O. Wertheim; Anton Nekturenko; Ben Murrell; Gordon W. Harkins; Philippe Lemey; Oscar A. MacLean; David L. Robertson; Tulio de Oliveira; Sergei L. Kosakovsky Pond; Matthew Bashton; Andrew Nelson; Clare McCann; Greg Young; Darren Smith

doi:10.1016/j.cell.2021.09.003

The emergence and ongoing convergent evolution of the SARS-CoV-2 N501Y lineages

NGS-SA, The COVID-19 Genomics UK (COG-UK) Consortium, Darren P. Martin^*, Steven Weaver, Houriiyah Tegally, James Emmanuel San, Stephen D. Shank, Eduan Wilkinson, Alexander G. Lucaci, Jennifer Giandhari, Sureshnee Naidoo, Yeshnee Pillay, Lavanya Singh, Richard J. Lessells, Ravindra K. Gupta, Joel O. Wertheim, Anton Nekturenko, Ben Murrell, Gordon W. Harkins, Philippe LemeyOscar A. MacLean, David L. Robertson, Tulio de Oliveira, Sergei L. Kosakovsky Pond, Matthew Bashton, Andrew Nelson, Clare McCann, Greg Young, Darren Smith

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

154 Citations (Scopus)

Abstract

The independent emergence late in 2020 of the B.1.1.7, B.1.351, and P.1 lineages of SARS-CoV-2 prompted renewed concerns about the evolutionary capacity of this virus to overcome public health interventions and rising population immunity. Here, by examining patterns of synonymous and non-synonymous mutations that have accumulated in SARS-CoV-2 genomes since the pandemic began, we find that the emergence of these three “501Y lineages” coincided with a major global shift in the selective forces acting on various SARS-CoV-2 genes. Following their emergence, the adaptive evolution of 501Y lineage viruses has involved repeated selectively favored convergent mutations at 35 genome sites, mutations we refer to as the 501Y meta-signature. The ongoing convergence of viruses in many other lineages on this meta-signature suggests that it includes multiple mutation combinations capable of promoting the persistence of diverse SARS-CoV-2 lineages in the face of mounting host immune recognition.

Original language	English
Pages (from-to)	5189-5200.e7
Number of pages	20
Journal	Cell
Volume	184
Issue number	20
Early online date	7 Sept 2021
DOIs	https://doi.org/10.1016/j.cell.2021.09.003
Publication status	Published - 30 Sept 2021

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

SDG 3 Good Health and Well-being

Keywords

convergent mutations
COVID 19
directional selection
diversifying selection
evolutionary adaptation
immune evasion
lineage-defining mutations
positive selection
recurrent mutations
transmission advantage

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10.1016/j.cell.2021.09.003

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NGS-SA, The COVID-19 Genomics UK (COG-UK) Consortium, Martin, D. P., Weaver, S., Tegally, H., San, J. E., Shank, S. D., Wilkinson, E., Lucaci, A. G., Giandhari, J., Naidoo, S., Pillay, Y., Singh, L., Lessells, R. J., Gupta, R. K., Wertheim, J. O., Nekturenko, A., Murrell, B., Harkins, G. W., ... Smith, D. (2021). The emergence and ongoing convergent evolution of the SARS-CoV-2 N501Y lineages. Cell, 184(20), 5189-5200.e7. https://doi.org/10.1016/j.cell.2021.09.003

@article{da53dec4cf0741779e4ab4b7128e8364,

title = "The emergence and ongoing convergent evolution of the SARS-CoV-2 N501Y lineages",

abstract = "The independent emergence late in 2020 of the B.1.1.7, B.1.351, and P.1 lineages of SARS-CoV-2 prompted renewed concerns about the evolutionary capacity of this virus to overcome public health interventions and rising population immunity. Here, by examining patterns of synonymous and non-synonymous mutations that have accumulated in SARS-CoV-2 genomes since the pandemic began, we find that the emergence of these three “501Y lineages” coincided with a major global shift in the selective forces acting on various SARS-CoV-2 genes. Following their emergence, the adaptive evolution of 501Y lineage viruses has involved repeated selectively favored convergent mutations at 35 genome sites, mutations we refer to as the 501Y meta-signature. The ongoing convergence of viruses in many other lineages on this meta-signature suggests that it includes multiple mutation combinations capable of promoting the persistence of diverse SARS-CoV-2 lineages in the face of mounting host immune recognition.",

keywords = "convergent mutations, COVID 19, directional selection, diversifying selection, evolutionary adaptation, immune evasion, lineage-defining mutations, positive selection, recurrent mutations, transmission advantage",

author = "NGS-SA and \{The COVID-19 Genomics UK (COG-UK) Consortium\} and Martin, \{Darren P.\} and Steven Weaver and Houriiyah Tegally and San, \{James Emmanuel\} and Shank, \{Stephen D.\} and Eduan Wilkinson and Lucaci, \{Alexander G.\} and Jennifer Giandhari and Sureshnee Naidoo and Yeshnee Pillay and Lavanya Singh and Lessells, \{Richard J.\} and Gupta, \{Ravindra K.\} and Wertheim, \{Joel O.\} and Anton Nekturenko and Ben Murrell and Harkins, \{Gordon W.\} and Philippe Lemey and MacLean, \{Oscar A.\} and Robertson, \{David L.\} and \{de Oliveira\}, Tulio and \{Kosakovsky Pond\}, \{Sergei L.\} and Matthew Bashton and Andrew Nelson and Clare McCann and Greg Young and Darren Smith",

note = "Matthew Bashton, Andrew Nelson, Clare McCann, Greg Young and Darren Smith are members of the COVID-19 Genomics UK (COG-UK) consortium. Funding information: The Wellcome Trust funded D.P.M. (222574/Z/21/Z), D.L.R. (220977/Z/20/Z), P.L. (2206298/Z/17/Z), and O.A.M. (206369/Z/17/Z). The US National Institutes of Health funded S.L.K.P. (R01 AI134384 and AI140970), J.O.W. (R01 AI13599), G.W.H. (1U01Al152151-01), and J.E.S. and H.T. (via H3ABioNet U24HG006941). The US National Science Foundation funded S.L.K.P. (RAPID 2027196 NSF/DBI,BIO), The UK Medical Research Council funded D.L.R. (MC\_UU\_1201412) and COG-UK (via UK Research \& Innovation, the National Institute of Health Research, and Genome Research Limited operating as the Wellcome Sanger Institute). The European Research Council funded P.L. (725422-ReservoirDOCS and 874850-MOOD). The South African Medical Research Council funded NGS-SA via the Strategic Health Innovation Partnerships Unit of the South African Medical Research Council and Department of Science and Innovation. ",

year = "2021",

month = sep,

day = "30",

doi = "10.1016/j.cell.2021.09.003",

language = "English",

volume = "184",

pages = "5189--5200.e7",

journal = "Cell",

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number = "20",

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NGS-SA, The COVID-19 Genomics UK (COG-UK) Consortium, Martin, DP, Weaver, S, Tegally, H, San, JE, Shank, SD, Wilkinson, E, Lucaci, AG, Giandhari, J, Naidoo, S, Pillay, Y, Singh, L, Lessells, RJ, Gupta, RK, Wertheim, JO, Nekturenko, A, Murrell, B, Harkins, GW, Lemey, P, MacLean, OA, Robertson, DL, de Oliveira, T, Kosakovsky Pond, SL, Bashton, M , Nelson, A , McCann, C, Young, G & Smith, D 2021, 'The emergence and ongoing convergent evolution of the SARS-CoV-2 N501Y lineages', Cell, vol. 184, no. 20, pp. 5189-5200.e7. https://doi.org/10.1016/j.cell.2021.09.003

TY - JOUR

T1 - The emergence and ongoing convergent evolution of the SARS-CoV-2 N501Y lineages

AU - NGS-SA

AU - The COVID-19 Genomics UK (COG-UK) Consortium

AU - Martin, Darren P.

AU - Weaver, Steven

AU - Tegally, Houriiyah

AU - San, James Emmanuel

AU - Shank, Stephen D.

AU - Wilkinson, Eduan

AU - Lucaci, Alexander G.

AU - Giandhari, Jennifer

AU - Naidoo, Sureshnee

AU - Pillay, Yeshnee

AU - Singh, Lavanya

AU - Lessells, Richard J.

AU - Gupta, Ravindra K.

AU - Wertheim, Joel O.

AU - Nekturenko, Anton

AU - Murrell, Ben

AU - Harkins, Gordon W.

AU - Lemey, Philippe

AU - MacLean, Oscar A.

AU - Robertson, David L.

AU - de Oliveira, Tulio

AU - Kosakovsky Pond, Sergei L.

AU - Bashton, Matthew

AU - Nelson, Andrew

AU - McCann, Clare

AU - Young, Greg

AU - Smith, Darren

N1 - Matthew Bashton, Andrew Nelson, Clare McCann, Greg Young and Darren Smith are members of the COVID-19 Genomics UK (COG-UK) consortium. Funding information: The Wellcome Trust funded D.P.M. (222574/Z/21/Z), D.L.R. (220977/Z/20/Z), P.L. (2206298/Z/17/Z), and O.A.M. (206369/Z/17/Z). The US National Institutes of Health funded S.L.K.P. (R01 AI134384 and AI140970), J.O.W. (R01 AI13599), G.W.H. (1U01Al152151-01), and J.E.S. and H.T. (via H3ABioNet U24HG006941). The US National Science Foundation funded S.L.K.P. (RAPID 2027196 NSF/DBI,BIO), The UK Medical Research Council funded D.L.R. (MC_UU_1201412) and COG-UK (via UK Research & Innovation, the National Institute of Health Research, and Genome Research Limited operating as the Wellcome Sanger Institute). The European Research Council funded P.L. (725422-ReservoirDOCS and 874850-MOOD). The South African Medical Research Council funded NGS-SA via the Strategic Health Innovation Partnerships Unit of the South African Medical Research Council and Department of Science and Innovation.

PY - 2021/9/30

Y1 - 2021/9/30

N2 - The independent emergence late in 2020 of the B.1.1.7, B.1.351, and P.1 lineages of SARS-CoV-2 prompted renewed concerns about the evolutionary capacity of this virus to overcome public health interventions and rising population immunity. Here, by examining patterns of synonymous and non-synonymous mutations that have accumulated in SARS-CoV-2 genomes since the pandemic began, we find that the emergence of these three “501Y lineages” coincided with a major global shift in the selective forces acting on various SARS-CoV-2 genes. Following their emergence, the adaptive evolution of 501Y lineage viruses has involved repeated selectively favored convergent mutations at 35 genome sites, mutations we refer to as the 501Y meta-signature. The ongoing convergence of viruses in many other lineages on this meta-signature suggests that it includes multiple mutation combinations capable of promoting the persistence of diverse SARS-CoV-2 lineages in the face of mounting host immune recognition.

AB - The independent emergence late in 2020 of the B.1.1.7, B.1.351, and P.1 lineages of SARS-CoV-2 prompted renewed concerns about the evolutionary capacity of this virus to overcome public health interventions and rising population immunity. Here, by examining patterns of synonymous and non-synonymous mutations that have accumulated in SARS-CoV-2 genomes since the pandemic began, we find that the emergence of these three “501Y lineages” coincided with a major global shift in the selective forces acting on various SARS-CoV-2 genes. Following their emergence, the adaptive evolution of 501Y lineage viruses has involved repeated selectively favored convergent mutations at 35 genome sites, mutations we refer to as the 501Y meta-signature. The ongoing convergence of viruses in many other lineages on this meta-signature suggests that it includes multiple mutation combinations capable of promoting the persistence of diverse SARS-CoV-2 lineages in the face of mounting host immune recognition.

KW - convergent mutations

KW - COVID 19

KW - directional selection

KW - diversifying selection

KW - evolutionary adaptation

KW - immune evasion

KW - lineage-defining mutations

KW - positive selection

KW - recurrent mutations

KW - transmission advantage

UR - https://www.scopus.com/pages/publications/85116536943

U2 - 10.1016/j.cell.2021.09.003

DO - 10.1016/j.cell.2021.09.003

M3 - Article

C2 - 33688681

AN - SCOPUS:85116536943

SN - 0092-8674

VL - 184

SP - 5189-5200.e7

JO - Cell

JF - Cell

IS - 20

ER -

The emergence and ongoing convergent evolution of the SARS-CoV-2 N501Y lineages

Abstract

UN SDGs

Keywords

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