IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-36001-5.html
   My bibliography  Save this article

Rapid transmission and tight bottlenecks constrain the evolution of highly transmissible SARS-CoV-2 variants

Author

Listed:
  • Emily E. Bendall

    (University of Michigan)

  • Amy P. Callear

    (University of Michigan)

  • Amy Getz

    (University of Michigan)

  • Kendra Goforth

    (University of Michigan)

  • Drew Edwards

    (University of Michigan)

  • Arnold S. Monto

    (University of Michigan)

  • Emily T. Martin

    (University of Michigan)

  • Adam S. Lauring

    (University of Michigan
    University of Michigan)

Abstract

Transmission bottlenecks limit the spread of novel mutations and reduce the efficiency of selection along a transmission chain. While increased force of infection, receptor binding, or immune evasion may influence bottleneck size, the relationship between transmissibility and the transmission bottleneck is unclear. Here we compare the transmission bottleneck of non-VOC SARS-CoV-2 lineages to those of Alpha, Delta, and Omicron. We sequenced viruses from 168 individuals in 65 households. Most virus populations had 0–1 single nucleotide variants (iSNV). From 64 transmission pairs with detectable iSNV, we identify a per clade bottleneck of 1 (95% CI 1–1) for Alpha, Delta, and Omicron and 2 (95% CI 2–2) for non-VOC. These tight bottlenecks reflect the low diversity at the time of transmission, which may be more pronounced in rapidly transmissible variants. Tight bottlenecks will limit the development of highly mutated VOC in transmission chains, adding to the evidence that selection over prolonged infections may drive their evolution.

Suggested Citation

  • Emily E. Bendall & Amy P. Callear & Amy Getz & Kendra Goforth & Drew Edwards & Arnold S. Monto & Emily T. Martin & Adam S. Lauring, 2023. "Rapid transmission and tight bottlenecks constrain the evolution of highly transmissible SARS-CoV-2 variants," Nature Communications, Nature, vol. 14(1), pages 1-7, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-36001-5
    DOI: 10.1038/s41467-023-36001-5
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-36001-5
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-023-36001-5?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Lucy G. Thorne & Mehdi Bouhaddou & Ann-Kathrin Reuschl & Lorena Zuliani-Alvarez & Ben Polacco & Adrian Pelin & Jyoti Batra & Matthew V. X. Whelan & Myra Hosmillo & Andrea Fossati & Roberta Ragazzini &, 2022. "Evolution of enhanced innate immune evasion by SARS-CoV-2," Nature, Nature, vol. 602(7897), pages 487-495, February.
    2. Lucy Dorp & Damien Richard & Cedric C. S. Tan & Liam P. Shaw & Mislav Acman & François Balloux, 2020. "No evidence for increased transmissibility from recurrent mutations in SARS-CoV-2," Nature Communications, Nature, vol. 11(1), pages 1-8, December.
    3. Bo Meng & Adam Abdullahi & Isabella A. T. M. Ferreira & Niluka Goonawardane & Akatsuki Saito & Izumi Kimura & Daichi Yamasoba & Pehuén Pereyra Gerber & Saman Fatihi & Surabhi Rathore & Samantha K. Zep, 2022. "Altered TMPRSS2 usage by SARS-CoV-2 Omicron impacts infectivity and fusogenicity," Nature, Nature, vol. 603(7902), pages 706-714, March.
    4. Baisheng Li & Aiping Deng & Kuibiao Li & Yao Hu & Zhencui Li & Yaling Shi & Qianling Xiong & Zhe Liu & Qianfang Guo & Lirong Zou & Huan Zhang & Meng Zhang & Fangzhu Ouyang & Juan Su & Wenzhe Su & Jing, 2022. "Viral infection and transmission in a large, well-traced outbreak caused by the SARS-CoV-2 Delta variant," Nature Communications, Nature, vol. 13(1), pages 1-9, December.
    5. Niyati Desai & Azfar Neyaz & Annamaria Szabolcs & Angela R. Shih & Jonathan H. Chen & Vishal Thapar & Linda T. Nieman & Alexander Solovyov & Arnav Mehta & David J. Lieb & Anupriya S. Kulkarni & Christ, 2020. "Temporal and spatial heterogeneity of host response to SARS-CoV-2 pulmonary infection," Nature Communications, Nature, vol. 11(1), pages 1-15, December.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Denis Mongin & Nils Bürgisser & Gustavo Laurie & Guillaume Schimmel & Diem-Lan Vu & Stephane Cullati & Delphine Sophie Courvoisier, 2023. "Effect of SARS-CoV-2 prior infection and mRNA vaccination on contagiousness and susceptibility to infection," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    2. Ana S. Gonzalez-Reiche & Hala Alshammary & Sarah Schaefer & Gopi Patel & Jose Polanco & Juan Manuel Carreño & Angela A. Amoako & Aria Rooker & Christian Cognigni & Daniel Floda & Adriana Guchte & Zain, 2023. "Sequential intrahost evolution and onward transmission of SARS-CoV-2 variants," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    3. Markus Hoffmann & Lok-Yin Roy Wong & Prerna Arora & Lu Zhang & Cheila Rocha & Abby Odle & Inga Nehlmeier & Amy Kempf & Anja Richter & Nico Joel Halwe & Jacob Schön & Lorenz Ulrich & Donata Hoffmann & , 2023. "Omicron subvariant BA.5 efficiently infects lung cells," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    4. Taha Y. Taha & Irene P. Chen & Jennifer M. Hayashi & Takako Tabata & Keith Walcott & Gabriella R. Kimmerly & Abdullah M. Syed & Alison Ciling & Rahul K. Suryawanshi & Hannah S. Martin & Bryan H. Bach , 2023. "Rapid assembly of SARS-CoV-2 genomes reveals attenuation of the Omicron BA.1 variant through NSP6," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    5. Guoli Shi & Tiansheng Li & Kin Kui Lai & Reed F. Johnson & Jonathan W. Yewdell & Alex A. Compton, 2024. "Omicron Spike confers enhanced infectivity and interferon resistance to SARS-CoV-2 in human nasal tissue," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    6. Jolien Van Cleemput & Willem van Snippenberg & Laurens Lambrechts & Amélie Dendooven & Valentino D’Onofrio & Liesbeth Couck & Wim Trypsteen & Jan Vanrusselt & Sebastiaan Theuns & Nick Vereecke & Thier, 2021. "Organ-specific genome diversity of replication-competent SARS-CoV-2," Nature Communications, Nature, vol. 12(1), pages 1-11, December.
    7. Biao Zhou & Runhong Zhou & Bingjie Tang & Jasper Fuk-Woo Chan & Mengxiao Luo & Qiaoli Peng & Shuofeng Yuan & Hang Liu & Bobo Wing-Yee Mok & Bohao Chen & Pui Wang & Vincent Kwok-Man Poon & Hin Chu & Ch, 2022. "A broadly neutralizing antibody protects Syrian hamsters against SARS-CoV-2 Omicron challenge," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    8. Nikhil Kumar Tulsian & Raghuvamsi Venkata Palur & Xinlei Qian & Yue Gu & Bhuvaneshwari D/O Shunmuganathan & Firdaus Samsudin & Yee Hwa Wong & Jianqing Lin & Kiren Purushotorman & Mary McQueen Kozma & , 2023. "Defining neutralization and allostery by antibodies against COVID-19 variants," Nature Communications, Nature, vol. 14(1), pages 1-23, December.
    9. Yuki Furuse, 2022. "Properties of the Omicron Variant of SARS-CoV-2 Affect Public Health Measure Effectiveness in the COVID-19 Epidemic," IJERPH, MDPI, vol. 19(9), pages 1-8, April.
    10. Juan Liu & Fengfeng Mao & Jianhe Chen & Shuaiyao Lu & Yonghe Qi & Yinyan Sun & Linqiang Fang & Man Lung Yeung & Chunmei Liu & Guimei Yu & Guangyu Li & Ximing Liu & Yuansheng Yao & Panpan Huang & Dongx, 2023. "An IgM-like inhalable ACE2 fusion protein broadly neutralizes SARS-CoV-2 variants," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    11. Lisa-Marie Funk & Gereon Poschmann & Fabian Rabe von Pappenheim & Ashwin Chari & Kim M. Stegmann & Antje Dickmanns & Marie Wensien & Nora Eulig & Elham Paknia & Gabi Heyne & Elke Penka & Arwen R. Pear, 2024. "Multiple redox switches of the SARS-CoV-2 main protease in vitro provide opportunities for drug design," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    12. Kaiyuan Sun & Stefano Tempia & Jackie Kleynhans & Anne Gottberg & Meredith L. McMorrow & Nicole Wolter & Jinal N. Bhiman & Jocelyn Moyes & Maimuna Carrim & Neil A. Martinson & Kathleen Kahn & Limakats, 2023. "Rapidly shifting immunologic landscape and severity of SARS-CoV-2 in the Omicron era in South Africa," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    13. Haofeng Wang & Qi Yang & Xiaoce Liu & Zili Xu & Maolin Shao & Dongxu Li & Yinkai Duan & Jielin Tang & Xianqiang Yu & Yumin Zhang & Aihua Hao & Yajie Wang & Jie Chen & Chenghao Zhu & Luke Guddat & Hong, 2023. "Structure-based discovery of dual pathway inhibitors for SARS-CoV-2 entry," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    14. Raffaele Palladino & Michelangelo Mercogliano & Claudio Fiorilla & Alessandro Frangiosa & Sabrina Iodice & Stefano Sanduzzi Zamparelli & Emma Montella & Maria Triassi & Alessandro Sanduzzi Zamparelli, 2022. "Association between COVID-19 and Sick Leave for Healthcare Workers in a Large Academic Hospital in Southern Italy: An Observational Study," IJERPH, MDPI, vol. 19(15), pages 1-8, August.
    15. Diana Rose E. Ranoa & Robin L. Holland & Fadi G. Alnaji & Kelsie J. Green & Leyi Wang & Richard L. Fredrickson & Tong Wang & George N. Wong & Johnny Uelmen & Sergei Maslov & Zachary J. Weiner & Alexei, 2022. "Mitigation of SARS-CoV-2 transmission at a large public university," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    16. Rong Zhu & Daniel Canena & Mateusz Sikora & Miriam Klausberger & Hannah Seferovic & Ahmad Reza Mehdipour & Lisa Hain & Elisabeth Laurent & Vanessa Monteil & Gerald Wirnsberger & Ralph Wieneke & Robert, 2022. "Force-tuned avidity of spike variant-ACE2 interactions viewed on the single-molecule level," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    17. Matthew J. Cummings & Barnabas Bakamutumaho & Julius J. Lutwama & Nicholas Owor & Xiaoyu Che & Maider Astorkia & Thomas S. Postler & John Kayiwa & Jocelyn Kiconco & Moses Muwanga & Christopher Nsereko, 2024. "COVID-19 immune signatures in Uganda persist in HIV co-infection and diverge by pandemic phase," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    18. Katherine U. Gaynor & Marina Vaysburd & Maximilian A. J. Harman & Anna Albecka & Phillip Jeffrey & Paul Beswick & Guido Papa & Liuhong Chen & Donna Mallery & Brian McGuinness & Katerine Rietschoten & , 2023. "Multivalent bicyclic peptides are an effective antiviral modality that can potently inhibit SARS-CoV-2," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    19. Adam Abdullahi & David Oladele & Michael Owusu & Steven A. Kemp & James Ayorinde & Abideen Salako & Douglas Fink & Fehintola Ige & Isabella A. T. M. Ferreira & Bo Meng & Augustina Angelina Sylverken &, 2022. "SARS-COV-2 antibody responses to AZD1222 vaccination in West Africa," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    20. Delphine Planas & Isabelle Staropoli & Vincent Michel & Frederic Lemoine & Flora Donati & Matthieu Prot & Francoise Porrot & Florence Guivel-Benhassine & Banujaa Jeyarajah & Angela Brisebarre & Océane, 2024. "Distinct evolution of SARS-CoV-2 Omicron XBB and BA.2.86/JN.1 lineages combining increased fitness and antibody evasion," Nature Communications, Nature, vol. 15(1), pages 1-17, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-36001-5. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.