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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
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    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. 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.
    3. 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.
    4. 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.
    5. 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.
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