Good genes but the wrong neighbors: Individual heterogeneity in disease susceptibility in House finches (Carpodacus mexicanus)

Individual heterogeneity in pathogen susceptibility is an often overlooked component of disease dynamics in wild populations that can have striking effects at broader ecological scales.  Despite the presence of substantial variation in disease response in natural populations, surprisingly few empirical studies have identified the ecological factors which contribute to this variation within and among host individuals.  Here I examine both intrinsic (genetic) and extrinsic (social behavior) factors that mediate host susceptibility to a recently emerged disease in eastern house finches (Carpodacus mexicanus). Since 1994, introduced populations of this North American bird species have experienced a debilitating disease epidemic caused by the bacterium Mycoplasma gallisepticum, with the highest disease prevalence occurring during periods of social flocking.  Here I examine how host genetic variation levels and social behavior mediate disease susceptibility in house finches at both individual and population scales.  First, I found that an individual’s neutral heterozygosity and Major Histocompability Complex variation predict the severity of disease susceptibility and host immunocompetence.  On a population scale, host genetic diversity levels correlate with broad geographic patterns of disease dynamics across the native and introduced species range.  Second, I manipulated social competition and an individual’s dominance status within house finch flocks and found that the social environment can directly influence immunocompetence and disease resistance: socially dominant house finches show stronger immunity and disease resistance under some competitive regimes, but not others.  Finally, social dominance and genetic variation are closely linked in this species, suggesting that variation in disease susceptibility is ultimately the result of complex gene-by-environment interactions.  Intrinsic and extrinsic ecological factors must be integrated in empirical studies of natural systems in order to understand host heterogeneity in disease susceptibility from a whole-organism perspective and the consequences of this variation at broader ecological scales.