Abstract
Disease acts as a powerful driver of evolution in natural host populations, yet individuals in a population often vary in their susceptibility to infection. Energetic trade‐offs between immune and reproductive investment lead to the evolution of distinct life history strategies, driven by the relative fitness costs and benefits of resisting infection. However, examples quantifying the cost of resistance outside of the laboratory are rare. Here, we observe two distinct forms of resistance to bovine tuberculosis (bTB), an important zoonotic pathogen, in a free‐ranging African buffalo (Syncerus caffer) population. We characterize these phenotypes as “infection resistance,” in which hosts delay or prevent infection, and “proliferation resistance,” in which the host limits the spread of lesions caused by the pathogen after infection has occurred. We found weak evidence that infection resistance to bTB may be heritable in this buffalo population (h 2 = 0.10) and comes at the cost of reduced body condition and marginally reduced survival once infected, but also associates with an overall higher reproductive rate. Infection‐resistant animals thus appear to follow a “fast” pace‐of‐life syndrome, in that they reproduce more quickly but die upon infection. In contrast, proliferation resistance had no apparent costs and was associated with measures of positive host health—such as having a higher body condition and reproductive rate. This study quantifies striking phenotypic variation in pathogen resistance and provides evidence for a link between life history variation and a disease resistance trait in a wild mammalian host population.
Highlights
Disease resistance traits can evolve rapidly as a result of coevolution between hosts and pathogens
This further complicates the study of coevolutionary dynamics within host populations, since selection acting on one resistance trait could affect the evolutionary trajectory of another (Ardia et al, 2011)
BTB was introduced into Southern Africa with European cattle, at this time, African buffalo serve as a maintenance host of bovine tuberculosis (bTB) in the region, sustaining a relatively high prevalence of M. bovis in some areas and facilitating infection of other hosts in the savanna ecosystem (Cross et al, 2009; Rodwell et al, 2001). bTB is most commonly transmitted through inhalation, colonizing lung and associated lymph tissues by infecting resident macrophages of the host (Kaufmann, 1991; Kornfeld, Mancino, & Colizzi, 1999; Raja, 2004)
Summary
Disease resistance traits can evolve rapidly as a result of coevolution between hosts and pathogens (van Valen, 1973). Since distinct resistance phenotypes likely arise from discrete underlying physiological mechanisms that carry unique fitness costs and benefits, multiple strategies could evolve within the same host population (Miller, White, & Boots, 2005; Restif & Koella, 2004). These resistance traits are not necessarily mutually exclusive and each individual occupies a phenotypic value along the continuum of each phenotype. Mycobacterium bovis is the causative agent of bovine tuberculosis (bTB) and a zoonotic bacterial pathogen with a broad host range, often leading to long‐term infection with high
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