Asynchrony between virus diversity and antibody selection limits influenza virus evolution

  1. Dylan H Morris  Is a corresponding author
  2. Velislava N Petrova
  3. Fernando W Rossine
  4. Edyth Parker
  5. Bryan T Grenfell
  6. Richard A Neher
  7. Simon A Levin
  8. Colin A Russell  Is a corresponding author
  1. Princeton University, United States
  2. Wellcome Sanger Institute, United Kingdom
  3. Academic Medical Center, University of Amsterdam, Netherlands
  4. University of Basel, Switzerland

Abstract

Seasonal influenza viruses create a persistent global disease burden by evolving to escape immunity induced by prior infections and vaccinations. New antigenic variants have a substantial selective advantage at the population level, but these variants are rarely selected within-host, even in previously immune individuals. Using a mathematical model, we show that the temporal asynchrony between within-host virus exponential growth and antibody-mediated selection could limit within-host antigenic evolution. If selection for new antigenic variants acts principally at the point of initial virus inoculation, where small virus populations encounter well-matched mucosal antibodies in previously infected individuals, there can exist protection against reinfection that does not regularly produce observable new antigenic variants within individual infected hosts. Our results provide a theoretical explanation for how virus antigenic evolution can be highly selective at the global level but nearly neutral within host. They also suggest new avenues for improving influenza control.

Data availability

All data used in this study are specifically listed in the appendix. No new primary data was generated in this study.

Article and author information

Author details

  1. Dylan H Morris

    Ecology and Evolutionary Biology, Princeton University, Princeton, United States
    For correspondence
    dhmorris@princeton.edu
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3655-406X
  2. Velislava N Petrova

    Human Genetics, Wellcome Sanger Institute, Cambridge, United Kingdom
    Competing interests
    No competing interests declared.
  3. Fernando W Rossine

    Ecology and Evolutionary Biology, Princeton University, Princeton, United States
    Competing interests
    No competing interests declared.
  4. Edyth Parker

    Department of Medical Microbiology, Academic Medical Center, University of Amsterdam, Amsterdam, Netherlands
    Competing interests
    No competing interests declared.
  5. Bryan T Grenfell

    Department of Ecology and Evolutionary Biology, Princeton University, Princeton, United States
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3227-5909
  6. Richard A Neher

    Biozentrum, University of Basel, Basel, Switzerland
    Competing interests
    Richard A Neher, Reviewing editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2525-1407
  7. Simon A Levin

    Department of Ecology and Evolutionary Biology, Princeton University, Princeton, United States
    Competing interests
    No competing interests declared.
  8. Colin A Russell

    Department of Medical Microbiology, Academic Medical Center, University of Amsterdam, Amsterdam, Netherlands
    For correspondence
    c.a.russell@amc.uva.nl
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2113-162X

Funding

H2020 European Research Council (Naviflu:818353)

  • Colin A Russell

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Armita Nourmohammad, University of Washington, United States

Version history

  1. Received: August 14, 2020
  2. Accepted: November 4, 2020
  3. Accepted Manuscript published: November 11, 2020 (version 1)
  4. Version of Record published: December 18, 2020 (version 2)

Copyright

© 2020, Morris et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Dylan H Morris
  2. Velislava N Petrova
  3. Fernando W Rossine
  4. Edyth Parker
  5. Bryan T Grenfell
  6. Richard A Neher
  7. Simon A Levin
  8. Colin A Russell
(2020)
Asynchrony between virus diversity and antibody selection limits influenza virus evolution
eLife 9:e62105.
https://doi.org/10.7554/eLife.62105

Share this article

https://doi.org/10.7554/eLife.62105

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