Evolution of host resistance and damage-limiting mechanisms to an emerging bacterial pathogen

Understanding how hosts minimise the cost of emerging infections has fundamental implications for epidemiological dynamics and the evolution of pathogen virulence. Despite this, few experimental studies conducted in natural populations have explicitly tested whether hosts evolve resistance, which prevents infections or reduces pathogen load through immune activation, or tolerance, which limits somatic damages without decreasing pathogen load. In addition, none have done so controlling for the virulence of the pathogen isolate used, despite critical effects on host responses to infection. Here, we conducted an experimental inoculation study to test whether eastern North American house finches (Haemorrhous mexicanus) have evolved resistance or tolerance to their emerging bacterial pathogen, Mycoplasma gallisepticum, using 55 distinct isolates of varying virulence. First, we show that peak pathogen loads, which occurred around 8 days post-inoculation, did not differ between experimentally inoculated finches from disease-exposed (eastern) versus unexposed (western) population. However, pathogen loads subsequently decreased faster and to a greater extent in finches from exposed populations, indicating that they were able to clear the infection through adaptive immune processes. Second, we found no between-population difference in the regression of clinical symptom severity on pathogen load; if tolerance had evolved then the slope of this regression is predicted to be shallower (less negative) in the exposed population. However, finches from exposed populations displayed lower symptom severity for a given pathogen load, suggesting that damage-limitation mechanisms have accompanied the evolution of immune clearance. These observations show that resistance and damage-limitation mechanisms - including, but not limited to the standard conceptualisation of tolerance - should not be seen as mutually exclusive. Nevertheless, we propose that host resistance is especially likely to evolve in response to pathogens such as M. gallisepticum that require virulence for successful infection and transmission.