Potential Downstream Immunological Effects of Evolved Disease Tolerance in House Finches

Emerging infectious diseases can exert strong selection on hosts to evolve resistance or tolerance to infection. However, it remains unknown whether the evolution of specific defense strategies against a novel pathogen influences host immune phenotypes more broadly, potentially affecting their ability to respond to other pathogens. In 1994 the bacterial pathogen, Mycoplasma gallisepticum (MG) jumped from poultry into house finches, causing severe conjunctivitis and reducing host survival. MG then spread across the continental United States, exerting strong selection on host populations and creating geographic variation in the degree of population co-evolutionary history with the pathogen. Prior work found that populations of house finches with longer histories of MG endemism have evolved tolerance and resistance to MG, and this evolution is associated with several immunological differences including reductions in pro-inflammatory immune responses. However, it remains unknown whether these immunological changes are limited to MG-specific defenses or whether broader immune responses differ between populations with distinct coevolutionary histories with MG. To examine possible effects of the evolution of host responses to MG, we used five immune assays to challenge house finches from four populations, ranging from no history of MG endemism to 20+ years of MG endemism. When challenged with phytohemagglutinin (PHA), populations differed significantly in the strength of wing web swelling, with populations with longer MG exposure (and thus the highest MG tolerance) on average exhibiting the weakest swelling response when mass differences were controlled for. However, detected population differences in wing web swelling were small, and population differences were absent for responses to four other immune assays that spanned components of the innate and adaptive immune system. Future work should examine whether the local inflammation that underlies swelling responses to PHA shares common immunological mechanisms with local inflammatory responses to MG, which may explain why populations with evolved tolerance to MG show slightly lower swelling responses in response to PHA. Overall, these results suggest that the evolution of MG tolerance may have minor downstream consequences for responses to certain antigens, with the potential to influence a host's ability to respond to novel pathogen challenges, but most components of the host immune system appear largely unaffected.