Data from: Rapid antagonistic coevolution in an emerging pathogen and its vertebrate host

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 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]. While inoculation with pathogen isolates from epidemic outbreak caused comparable sub-lethal eye-swelling in hosts from exposed (hereafter adapted) and unexposed (hereafter ancestral) populations, inoculation 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.

宿主-病原体协同进化 (host-pathogen coevolution) 被认为在生态进化过程 (eco-evolutionary processes) 中扮演关键角色，涵盖流行病学动态 (epidemiological dynamics) 与有性生殖的演化[1-4]。尽管如此，宿主-病原体协同进化的直接证据仍极为稀缺[5-7]，在脊椎动物宿主中尤为突出。诚然，尽管已有研究证实脊椎动物宿主会响应病原体产生适应性演化，抑或病原体响应宿主发生演化[8-12]，但关于两类拮抗生物随时间推移在适合度层面发生必要互惠性变化的直接证据仍寥寥无几[13]。本研究通过时间移置实验 (time-shift experiment)，证实了北美家朱雀 (*Haemorhous mexicanus*) 与其细菌性病原体鸡毒支原体 (*Mycoplasma gallisepticum*) 之间存在适应性互惠演化[14-16]。本实验设计得以实现，得益于两类已被充分研究的朱雀种群：一类已暴露于病原体，另一类未暴露；在前者种群近期扩散遗传抗性之前，二者对实验接种的响应被证实并无显著差异[14,17]。当使用流行病暴发时期分离的病原体菌株进行接种时，来自已暴露（下称“适应性种群”）与未暴露（下称“祖先种群”）的宿主均出现了程度相当的亚致死性眼部肿胀；而使用抗性扩散后分离的菌株进行接种时，祖先种群宿主出现致死症状的概率是适应性种群的三倍。类似地，当使用近期分离的菌株接种祖先种群宿主时，病原体成功在原宿主中建立感染，并在诱导宿主死亡前传播至未感染哨兵宿主的概率最高；而使用早期分离的菌株接种适应性种群宿主时，该概率最低。本研究结果证实了拮抗性宿主-病原体协同进化的存在：宿主与病原体随时间推移分别演化出了更强的抗性与毒力，以响应对方的适应性变化。