Experimental evidence for distinct costs of pathogenesis and immunity against a natural pathogen in a wild bird

Protective immunity is expected to evolve when the costs of mounting an immune response are less than those of harbouring pathogens. Estimating the costs of immunity vs. pathogenesis in natural systems is challenging, however, because they are typically closely linked. Here we attempt to disentangle the relative cost of each using experimental infections in a natural host-parasite system in which hosts (house finches, Carpodacus mexicanus) differ in resistance to a bacterium (Mycoplasma gallisepticum, MG), depending on whether they originate from co-evolved or unexposed populations. Experimental infection with a 2007-strain of MG caused finches from co-evolved populations to lose significantly more mass relative to controls, than those from unexposed populations. In addition, infected co-evolved finches that lost the most mass harboured the least amounts of MG, whereas the reverse was true in finches from unexposed populations. Finally, within co-evolved populations, individuals that displayed transcriptional evidence of higher protective immune activity, as indicated by changes in the expression of candidate immune and immune-related genes in a direction consistent with increased resistance to MG, showed greater mass loss and lower MG load. Thus, mass loss appeared to reflect the costs of immunity vs. pathogenesis in co-evolved and unexposed populations, respectively. Our results suggest that resistance can evolve even when the short-term energetic costs of protective immunity exceed those of pathogenesis, providing the longer-term fitness costs of infection are sufficiently high.