Contrasting evolution of virulence and replication rate in an emerging bacterial pathogen

Luc Tardy, Mathieu Giraudeau, Geoffrey E. Hill, Kevin McGraw, Camille Bonneaud

Research output: Contribution to journalArticle

Abstract

Host resistance through immune clearance is predicted to favor pathogens that are able to transmit faster and are hence more virulent. Increasing pathogen virulence is, in turn, typically assumed to be mediated by increasing replication rates. However, experiments designed to test how pathogen virulence and replication rates evolve in response to increasing host resistance, as well as the relationship between the two, are rare and lacking for naturally evolving host–pathogen interactions. We inoculated 55 isolates of Mycoplasma gallisepticum, collected over 20 y from outbreak, into house finches (Haemorhous mexicanus) from disease-unexposed populations, which have not evolved protective immunity to M. gallisepticum. We show using 3 different metrics of virulence (body mass loss, symptom severity, and putative mortality rate) that virulence has increased linearly over >150,000 bacterial generations since outbreak (1994 to 2015). By contrast, while replication rates increased from outbreak to the initial spread of resistance (1994 to 2004), no further increases have occurred subsequently (2007 to 2015). Finally, as a consequence, we found that any potential mediating effect of replication rate on virulence evolution was restricted to the period when host resistance was initially increasing in the population. Taken together, our results show that pathogen virulence and replication rates can evolve independently, particularly after the initial spread of host resistance. We hypothesize that the evolution of pathogen virulence can be driven primarily by processes such as immune manipulation after resistance spreads in host populations.

Original languageEnglish (US)
Pages (from-to)16927-16932
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume116
Issue number34
DOIs
StatePublished - Aug 20 2019

Fingerprint

Virulence
Mycoplasma gallisepticum
Disease Outbreaks
Population
Finches
Immunity
Mortality

Keywords

  • Bacteria
  • Emerging infectious disease
  • Evolution of resistance
  • Evolution of virulence
  • Pathogen loa

ASJC Scopus subject areas

  • General

Cite this

Contrasting evolution of virulence and replication rate in an emerging bacterial pathogen. / Tardy, Luc; Giraudeau, Mathieu; Hill, Geoffrey E.; McGraw, Kevin; Bonneaud, Camille.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 116, No. 34, 20.08.2019, p. 16927-16932.

Research output: Contribution to journalArticle

Tardy, Luc ; Giraudeau, Mathieu ; Hill, Geoffrey E. ; McGraw, Kevin ; Bonneaud, Camille. / Contrasting evolution of virulence and replication rate in an emerging bacterial pathogen. In: Proceedings of the National Academy of Sciences of the United States of America. 2019 ; Vol. 116, No. 34. pp. 16927-16932.
@article{db3608007cbc43b985842c95eb556df7,
title = "Contrasting evolution of virulence and replication rate in an emerging bacterial pathogen",
abstract = "Host resistance through immune clearance is predicted to favor pathogens that are able to transmit faster and are hence more virulent. Increasing pathogen virulence is, in turn, typically assumed to be mediated by increasing replication rates. However, experiments designed to test how pathogen virulence and replication rates evolve in response to increasing host resistance, as well as the relationship between the two, are rare and lacking for naturally evolving host–pathogen interactions. We inoculated 55 isolates of Mycoplasma gallisepticum, collected over 20 y from outbreak, into house finches (Haemorhous mexicanus) from disease-unexposed populations, which have not evolved protective immunity to M. gallisepticum. We show using 3 different metrics of virulence (body mass loss, symptom severity, and putative mortality rate) that virulence has increased linearly over >150,000 bacterial generations since outbreak (1994 to 2015). By contrast, while replication rates increased from outbreak to the initial spread of resistance (1994 to 2004), no further increases have occurred subsequently (2007 to 2015). Finally, as a consequence, we found that any potential mediating effect of replication rate on virulence evolution was restricted to the period when host resistance was initially increasing in the population. Taken together, our results show that pathogen virulence and replication rates can evolve independently, particularly after the initial spread of host resistance. We hypothesize that the evolution of pathogen virulence can be driven primarily by processes such as immune manipulation after resistance spreads in host populations.",
keywords = "Bacteria, Emerging infectious disease, Evolution of resistance, Evolution of virulence, Pathogen loa",
author = "Luc Tardy and Mathieu Giraudeau and Hill, {Geoffrey E.} and Kevin McGraw and Camille Bonneaud",
year = "2019",
month = "8",
day = "20",
doi = "10.1073/pnas.1901556116",
language = "English (US)",
volume = "116",
pages = "16927--16932",
journal = "Proceedings of the National Academy of Sciences of the United States of America",
issn = "0027-8424",
number = "34",

}

TY - JOUR

T1 - Contrasting evolution of virulence and replication rate in an emerging bacterial pathogen

AU - Tardy, Luc

AU - Giraudeau, Mathieu

AU - Hill, Geoffrey E.

AU - McGraw, Kevin

AU - Bonneaud, Camille

PY - 2019/8/20

Y1 - 2019/8/20

N2 - Host resistance through immune clearance is predicted to favor pathogens that are able to transmit faster and are hence more virulent. Increasing pathogen virulence is, in turn, typically assumed to be mediated by increasing replication rates. However, experiments designed to test how pathogen virulence and replication rates evolve in response to increasing host resistance, as well as the relationship between the two, are rare and lacking for naturally evolving host–pathogen interactions. We inoculated 55 isolates of Mycoplasma gallisepticum, collected over 20 y from outbreak, into house finches (Haemorhous mexicanus) from disease-unexposed populations, which have not evolved protective immunity to M. gallisepticum. We show using 3 different metrics of virulence (body mass loss, symptom severity, and putative mortality rate) that virulence has increased linearly over >150,000 bacterial generations since outbreak (1994 to 2015). By contrast, while replication rates increased from outbreak to the initial spread of resistance (1994 to 2004), no further increases have occurred subsequently (2007 to 2015). Finally, as a consequence, we found that any potential mediating effect of replication rate on virulence evolution was restricted to the period when host resistance was initially increasing in the population. Taken together, our results show that pathogen virulence and replication rates can evolve independently, particularly after the initial spread of host resistance. We hypothesize that the evolution of pathogen virulence can be driven primarily by processes such as immune manipulation after resistance spreads in host populations.

AB - Host resistance through immune clearance is predicted to favor pathogens that are able to transmit faster and are hence more virulent. Increasing pathogen virulence is, in turn, typically assumed to be mediated by increasing replication rates. However, experiments designed to test how pathogen virulence and replication rates evolve in response to increasing host resistance, as well as the relationship between the two, are rare and lacking for naturally evolving host–pathogen interactions. We inoculated 55 isolates of Mycoplasma gallisepticum, collected over 20 y from outbreak, into house finches (Haemorhous mexicanus) from disease-unexposed populations, which have not evolved protective immunity to M. gallisepticum. We show using 3 different metrics of virulence (body mass loss, symptom severity, and putative mortality rate) that virulence has increased linearly over >150,000 bacterial generations since outbreak (1994 to 2015). By contrast, while replication rates increased from outbreak to the initial spread of resistance (1994 to 2004), no further increases have occurred subsequently (2007 to 2015). Finally, as a consequence, we found that any potential mediating effect of replication rate on virulence evolution was restricted to the period when host resistance was initially increasing in the population. Taken together, our results show that pathogen virulence and replication rates can evolve independently, particularly after the initial spread of host resistance. We hypothesize that the evolution of pathogen virulence can be driven primarily by processes such as immune manipulation after resistance spreads in host populations.

KW - Bacteria

KW - Emerging infectious disease

KW - Evolution of resistance

KW - Evolution of virulence

KW - Pathogen loa

UR - http://www.scopus.com/inward/record.url?scp=85071268298&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85071268298&partnerID=8YFLogxK

U2 - 10.1073/pnas.1901556116

DO - 10.1073/pnas.1901556116

M3 - Article

VL - 116

SP - 16927

EP - 16932

JO - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

SN - 0027-8424

IS - 34

ER -