TY - JOUR
T1 - Rapid Antagonistic Coevolution in an Emerging Pathogen and Its Vertebrate Host
AU - Bonneaud, Camille
AU - Giraudeau, Mathieu
AU - Tardy, Luc
AU - Staley, Molly
AU - Hill, Geoffrey E.
AU - McGraw, Kevin
N1 - Funding Information:
This research was supported by a Natural Environment Research Council standard grant ( NE/M00256X to C.B.). We thank A. Russell, A. Buckling, D. Ebert, and three anonymous referees for helpful discussion and/or constructive comments on the manuscript. We thank M. Cooke for assisting with bird captures in Arizona, A. Santos and undergraduates in the lab of W.R. Hood for assisting with bird captures in Alabama, and A.K. Ziegler for assisting with the experiment in Arizona.
Publisher Copyright:
© 2018 The Authors
PY - 2018/9/24
Y1 - 2018/9/24
N2 - Host-pathogen coevolution is assumed to play a key role in eco-evolutionary processes, including epidemiological dynamics and the evolution of sexual reproduction [1–4]. Despite this, direct evidence for host-pathogen coevolution is exceptional [5–7], particularly in vertebrate hosts. Indeed, although vertebrate hosts have been shown to evolve in response to pathogens or vice versa [8–12], there is little evidence for the necessary reciprocal changes in the success of both antagonists over time [13]. Here, we generate a time-shift experiment to demonstrate adaptive, reciprocal changes in North American house finches (Haemorhous mexicanus) and their emerging bacterial pathogen, Mycoplasma gallisepticum [14–16]. Our experimental design is made possible by the existence of disease-exposed and unexposed finch populations, which were known to exhibit equivalent responses to experimental inoculation until the recent spread of genetic resistance in the former [14, 17]. Whereas inoculations with pathogen isolates from epidemic outbreak caused comparable sub-lethal eye swelling in hosts from exposed (hereafter adapted) and unexposed (hereafter ancestral) populations, inoculations with isolates sampled after the spread of resistance were threefold more likely to cause lethal symptoms in hosts from ancestral populations. Similarly, the probability that pathogens successfully established an infection in the primary host and, before inducing death, transmitted to an uninfected sentinel was highest when recent isolates were inoculated in hosts from ancestral populations and lowest when early isolates were inoculated in hosts from adapted populations. Our results demonstrate antagonistic host-pathogen coevolution, with hosts and pathogens displaying increased resistance and virulence in response to each other over time. Bonneaud et al. provide a rare demonstration that hosts and pathogens evolve in response to each other. House finches have evolved increased resistance to their emerging pathogen, while the pathogen has evolved increased virulence in response. Our results have implications for pathogen evolution in response to resistance through antibiotics.
AB - Host-pathogen coevolution is assumed to play a key role in eco-evolutionary processes, including epidemiological dynamics and the evolution of sexual reproduction [1–4]. Despite this, direct evidence for host-pathogen coevolution is exceptional [5–7], particularly in vertebrate hosts. Indeed, although vertebrate hosts have been shown to evolve in response to pathogens or vice versa [8–12], there is little evidence for the necessary reciprocal changes in the success of both antagonists over time [13]. Here, we generate a time-shift experiment to demonstrate adaptive, reciprocal changes in North American house finches (Haemorhous mexicanus) and their emerging bacterial pathogen, Mycoplasma gallisepticum [14–16]. Our experimental design is made possible by the existence of disease-exposed and unexposed finch populations, which were known to exhibit equivalent responses to experimental inoculation until the recent spread of genetic resistance in the former [14, 17]. Whereas inoculations with pathogen isolates from epidemic outbreak caused comparable sub-lethal eye swelling in hosts from exposed (hereafter adapted) and unexposed (hereafter ancestral) populations, inoculations with isolates sampled after the spread of resistance were threefold more likely to cause lethal symptoms in hosts from ancestral populations. Similarly, the probability that pathogens successfully established an infection in the primary host and, before inducing death, transmitted to an uninfected sentinel was highest when recent isolates were inoculated in hosts from ancestral populations and lowest when early isolates were inoculated in hosts from adapted populations. Our results demonstrate antagonistic host-pathogen coevolution, with hosts and pathogens displaying increased resistance and virulence in response to each other over time. Bonneaud et al. provide a rare demonstration that hosts and pathogens evolve in response to each other. House finches have evolved increased resistance to their emerging pathogen, while the pathogen has evolved increased virulence in response. Our results have implications for pathogen evolution in response to resistance through antibiotics.
KW - bacteria
KW - emerging infectious disease
KW - evolution of resistance
KW - evolution of virulence
KW - host shift
KW - time-shift experiment
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U2 - 10.1016/j.cub.2018.07.003
DO - 10.1016/j.cub.2018.07.003
M3 - Article
C2 - 30197084
AN - SCOPUS:85052921375
SN - 0960-9822
VL - 28
SP - 2978-2983.e5
JO - Current Biology
JF - Current Biology
IS - 18
ER -