Evolutionary emergence of infectious diseases in heterogeneous host populations.

The emergence and re-emergence of pathogens remains a major public health concern. Unfortunately, when and where pathogens will (re-)emerge is notoriously difficult to predict, as the erratic nature of those events is reinforced by the stochastic nature of pathogen evolution during the early phase o...

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Main Authors: Hélène Chabas, Sébastien Lion, Antoine Nicot, Sean Meaden, Stineke van Houte, Sylvain Moineau, Lindi M Wahl, Edze R Westra, Sylvain Gandon
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2018-09-01
Series:PLoS Biology
Online Access:http://europepmc.org/articles/PMC6171948?pdf=render
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spelling doaj-54a86ab65d064ce1a8cf60aa3525630f2021-07-02T01:15:08ZengPublic Library of Science (PLoS)PLoS Biology1544-91731545-78852018-09-01169e200673810.1371/journal.pbio.2006738Evolutionary emergence of infectious diseases in heterogeneous host populations.Hélène ChabasSébastien LionAntoine NicotSean MeadenStineke van HouteSylvain MoineauLindi M WahlEdze R WestraSylvain GandonThe emergence and re-emergence of pathogens remains a major public health concern. Unfortunately, when and where pathogens will (re-)emerge is notoriously difficult to predict, as the erratic nature of those events is reinforced by the stochastic nature of pathogen evolution during the early phase of an epidemic. For instance, mutations allowing pathogens to escape host resistance may boost pathogen spread and promote emergence. Yet, the ecological factors that govern such evolutionary emergence remain elusive because of the lack of ecological realism of current theoretical frameworks and the difficulty of experimentally testing their predictions. Here, we develop a theoretical model to explore the effects of the heterogeneity of the host population on the probability of pathogen emergence, with or without pathogen evolution. We show that evolutionary emergence and the spread of escape mutations in the pathogen population is more likely to occur when the host population contains an intermediate proportion of resistant hosts. We also show that the probability of pathogen emergence rapidly declines with the diversity of resistance in the host population. Experimental tests using lytic bacteriophages infecting their bacterial hosts containing Clustered Regularly Interspaced Short Palindromic Repeat and CRISPR-associated (CRISPR-Cas) immune defenses confirm these theoretical predictions. These results suggest effective strategies for cross-species spillover and for the management of emerging infectious diseases.http://europepmc.org/articles/PMC6171948?pdf=render
collection DOAJ
language English
format Article
sources DOAJ
author Hélène Chabas
Sébastien Lion
Antoine Nicot
Sean Meaden
Stineke van Houte
Sylvain Moineau
Lindi M Wahl
Edze R Westra
Sylvain Gandon
spellingShingle Hélène Chabas
Sébastien Lion
Antoine Nicot
Sean Meaden
Stineke van Houte
Sylvain Moineau
Lindi M Wahl
Edze R Westra
Sylvain Gandon
Evolutionary emergence of infectious diseases in heterogeneous host populations.
PLoS Biology
author_facet Hélène Chabas
Sébastien Lion
Antoine Nicot
Sean Meaden
Stineke van Houte
Sylvain Moineau
Lindi M Wahl
Edze R Westra
Sylvain Gandon
author_sort Hélène Chabas
title Evolutionary emergence of infectious diseases in heterogeneous host populations.
title_short Evolutionary emergence of infectious diseases in heterogeneous host populations.
title_full Evolutionary emergence of infectious diseases in heterogeneous host populations.
title_fullStr Evolutionary emergence of infectious diseases in heterogeneous host populations.
title_full_unstemmed Evolutionary emergence of infectious diseases in heterogeneous host populations.
title_sort evolutionary emergence of infectious diseases in heterogeneous host populations.
publisher Public Library of Science (PLoS)
series PLoS Biology
issn 1544-9173
1545-7885
publishDate 2018-09-01
description The emergence and re-emergence of pathogens remains a major public health concern. Unfortunately, when and where pathogens will (re-)emerge is notoriously difficult to predict, as the erratic nature of those events is reinforced by the stochastic nature of pathogen evolution during the early phase of an epidemic. For instance, mutations allowing pathogens to escape host resistance may boost pathogen spread and promote emergence. Yet, the ecological factors that govern such evolutionary emergence remain elusive because of the lack of ecological realism of current theoretical frameworks and the difficulty of experimentally testing their predictions. Here, we develop a theoretical model to explore the effects of the heterogeneity of the host population on the probability of pathogen emergence, with or without pathogen evolution. We show that evolutionary emergence and the spread of escape mutations in the pathogen population is more likely to occur when the host population contains an intermediate proportion of resistant hosts. We also show that the probability of pathogen emergence rapidly declines with the diversity of resistance in the host population. Experimental tests using lytic bacteriophages infecting their bacterial hosts containing Clustered Regularly Interspaced Short Palindromic Repeat and CRISPR-associated (CRISPR-Cas) immune defenses confirm these theoretical predictions. These results suggest effective strategies for cross-species spillover and for the management of emerging infectious diseases.
url http://europepmc.org/articles/PMC6171948?pdf=render
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