Rapid Antagonistic Coevolution in an Emerging Pathogen and Its Vertebrate Host

Camille Bonneaud,Mathieu Giraudeau,Luc Tardy,Molly Staley,Geoffrey E Hill,Kevin J Mcgraw

doi:10.1016/j.cub.2018.07.003

Camille Bonneaud, Mathieu Giraudeau + Show 4 more

Open Access

https://doi.org/10.1016/j.cub.2018.07.003

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Abstract

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.

Highlights

Here we generated a ‘‘time-shift’’ experimental design by inoculating birds from exposed (hereafter adapted) and unexposed (hereafter ancestral) populations with 55 bacterial isolates sampled over the course the epidemic, from 1994 (i.e., initial outbreak), through the spread of host resistance (i.e., by $2007) [14], to 2015 (i.e., when the experiment was performed)
In support of pathogen evolution, we found that the probability of hosts developing conjunctivitis increased as a function of the year of pathogen sampling (Figure 1A; 1st part of hurdle model: mixed effect logistic regression, estimate ± SE = 0.4 ± 0.1, z = 3.5, p < 0.0005), but did not differ significantly between hosts from adapted versus ancestral populations
The second part of the model tested for differences in the severity of the infection in symptomatic hosts. In support of both pathogen and host evolution, we found that the peak clinical severity of symptomatic hosts increased when inoculated with pathogens sampled later in the epidemic (Figure 1B; 2nd part of hurdle model: linear mixed effect model, estimate ± SE = 0.03 ± 0.01, c2 = 11.6, degrees of freedom [df] = 1, p < 0.001) and was, as expected, significantly higher in hosts from ancestral populations. These results demonstrate that (1) pathogen virulence has increased over the course of the epidemic, and (2) hosts from adapted and ancestral populations were likely to become infected, those from the former were subsequently better able to resist the infection

Summary

Introduction

Here we generated a ‘‘time-shift’’ experimental design by inoculating birds from exposed (hereafter adapted) and unexposed (hereafter ancestral) populations with 55 bacterial isolates sampled over the course the epidemic, from 1994 (i.e., initial outbreak), through the spread of host resistance (i.e., by $2007) [14], to 2015 (i.e., when the experiment was performed). The first part tested whether inoculation with pathogen isolates sampled from varying time points during the epidemic had differential effects on the probability of the infection overall, and whether there were differences for hosts from adapted versus ancestral populations.

Results

Conclusion