Phylodynamic theory of persistence, extinction and speciation of rapidly adapting pathogens

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Abstract

Rapidly evolving pathogens like influenza viruses can persist by changing their antigenic properties fast enough to evade the adaptive immunity, yet they rarely split into diverging lineages. By mapping the multi-strain Susceptible-Infected-Recovered model onto the traveling wave model of adapting populations, we demonstrate that persistence of a rapidly evolving, Red-Queen-like state of the pathogen population requires long-ranged cross-immunity and sufficiently large population sizes. This state is unstable and the population goes extinct or 'speciates' into two pathogen strains with antigenic divergence beyond the range of cross-inhibition. However, in a certain range of evolutionary parameters, a single cross-inhibiting population can exist for times long compared to the time to the most recent common ancestor (T_MRCA) and gives rise to phylogenetic patterns typical of influenza virus. We demonstrate that the rate of speciation is related to fluctuations of T_MRCA and construct a 'phase diagram' identifying different phylodynamic regimes as a function of evolutionary parameters.

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Computer programs used for numerical simulations and analysis have been made publicly available athttps://github.com/neherlab/FluSpeciation

Article and author information

Author details

Le Yan

Kavli Institute for Theoretical Physics, University of California, Santa Barbara, Santa Barbara, United States

For correspondence
lyan@kitp.ucsb.edu

Competing interests
No competing interests declared.
Richard A Neher

Biozentrum, University of Basel, Basel, Switzerland

For correspondence
richard.neher@unibas.ch

Competing interests
Richard A Neher, Reviewing editor, eLife.

"This ORCID iD identifies the author of this article:" 0000-0003-2525-1407
Boris I Shraiman

Kavli Institute for Theoretical Physics, University of California, Santa Barbara, Santa Barbara, United States

For correspondence
shraiman@kitp.ucsb.edu

Competing interests
No competing interests declared.

"This ORCID iD identifies the author of this article:" 0000-0003-0886-8990

Funding

Simons Foundation (326844)

Boris I Shraiman

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

Copyright

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.