Rapid adaptation to a novel pathogen through disease tolerance in a wild songbird

Author summaryWhen organisms encounter a novel pathogen, they can adapt to it in two ways: by killing the pathogen (known as resistance) or reducing the damage incurred while not directly killing the pathogen (known as disease tolerance). Although much work has focused on resistance, we understand less about how animals achieve disease tolerance or how quickly disease tolerance can evolve. Here we show that a wild bird species (the house finch) has evolved disease tolerance to a novel bacterial pathogen quickly (within similar to 20-25 years, at most similar to 15 generations). In house finches, this pathogen causes severe swelling around the eye and limits their ability to avoid predators. House finch populations that have evolved with this pathogen for longer are more tolerant to it; they show milder eye swelling even though they do not clear the pathogen any more efficiently than their less-tolerant counterparts. Moreover, tolerant finches have fewer immune genes that turn on in response to the infection, suggesting that a more-targeted immune response may facilitate tolerance. As disease tolerance can potentially help humans and animals adapt to new pathogens and also may change the way pathogens spread through animal populations, it is critical we understand how, and how quickly, tolerance evolves. Animal hosts can adapt to emerging infectious disease through both disease resistance, which decreases pathogen numbers, and disease tolerance, which limits damage during infection without limiting pathogen replication. Both resistance and tolerance mechanisms can drive pathogen transmission dynamics. However, it is not well understood how quickly host tolerance evolves in response to novel pathogens or what physiological mechanisms underlie this defense. Using natural populations of house finches (Haemorhous mexicanus) across the temporal invasion gradient of a recently emerged bacterial pathogen (Mycoplasma gallisepticum), we find rapid evolution of tolerance (<25 years). In particular, populations with a longer history of MG endemism have less pathology but similar pathogen loads compared with populations with a shorter history of MG endemism. Further, gene expression data reveal that more-targeted immune responses early in infection are associated with tolerance. These results suggest an important role for tolerance in host adaptation to emerging infectious diseases, a phenomenon with broad implications for pathogen spread and evolution.