Incomplete host immunity favors the evolution of virulence in an emergent pathogen

Immune memory evolved to protect hosts from reinfection, but incomplete responses that allow future reinfection might inadvertently select for more harmful pathogens. We present empirical and modeling evidence that incomplete immunity promotes the evolution of higher virulence in a natural host-pathogen system. We performed sequential infections of house finches with Mycoplasma gallisepticum strains of varying virulence. Virulent bacterial strains generated stronger host protection against reinfection than less virulent strains, and thus excluded less virulent strains from infecting previously-exposed hosts. In a two-strain model, the resulting fitness advantage selected for an almost two-fold increase in pathogen virulence. Thus, the same immune systems that protect hosts from infection can concomitantly drive the evolution of more harmful pathogens in nature.

免疫记忆的演化本是为了保护宿主免受再次感染，但无法完全清除病原体、允许后续再次感染的不完全免疫应答，可能会无意间筛选出毒性更强的病原体。本研究提供实验与建模证据，证明在自然宿主-病原体系统（host-pathogen system）中，不完全免疫会推动更高毒力的演化。我们以不同毒力的鸡毒支原体（Mycoplasma gallisepticum）菌株对家朱雀开展连续感染实验。相较于低毒力菌株，高毒力的细菌菌株能为宿主提供更强的再次感染防护能力，因此可将低毒力菌株排除在已暴露宿主的感染范围之外。在双菌株模型中，由此产生的适合度优势会促使病原体毒力提升近两倍。由此可见，本应保护宿主免受感染的免疫系统，在自然环境中可能同时推动了毒性更强病原体的演化。