The immune system plays a critical role in maintaining overall health and keeping parasites at bay. While investment in immune function may improve survival, it may also come at a cost to reproduction, either because of limited resources or an over-reactive immune system attacking the body. Here, the authors aim to explore the evidence for relationships between immune investment, disease severity, survival, and reproduction in a wild population of gray wolves. Gray wolves were reintroduced into Yellowstone National Park in 1995, and within this population, researchers have studied the natural process of parasite infections. This work has shown that individual wolves vary in their response to infection with canine distemper virus and sarcoptic mange, despite the high survival-costs associated with an inability to control infection. None of this variation is explained by host characteristics such as age, sex, and social status. This project will test the hypothesis that a tradeoff between immune function and reproduction explains the maintenance of immune variation among individuals. Several indices of immune investment (natural antibodies, specific antibodies, and total antibodies) will be measured as predictors of disease severity and survival through known disease outbreaks. This information will be matched to reproductive fitness in order to test whether increased immune responsiveness comes at a cost to reproduction. This work will further test the specific prediction that costs to reproduction occur in the form of decreased litter sizes, and that these costs may be offset during disease outbreaks in the form of increased litter survival.
Results from this research will improve our understanding of the mechanisms by which variation in immune function is maintained in wildlife populations, which has important applications in conservation biology and wildlife management. The project will build on a rich, long-term public dataset on a wild carnivore being reintroduced to national parks, and will further our understanding of the drivers of an iconic conservation species. Results from this study will be published on a citizen science website, and disseminated via public lectures through the National Park Service and to school groups. This study will also expand the research training and skill sets of a doctoral student.
Despite the strong selective pressure that parasites place on their hosts, hosts still vary in their ability to mount an immune response and control infections. The central challenge faced by the field of ecoimmunology has been to understand causes of this variation and consequences for host fitness (Graham et al. 2011, Hawley and Altizer 2011). Costs associated with mounting or maintaining an immune response are thought to underpin much of this variation, driving trade-offs with other life-history needs such as reproduction and growth (Sheldon and Verhulst 1996, Graham et al. 2010, Mills et al. 2010). Variable parasite pressures and genetic and environmental variation are further expected to shape an individual’s immune response or optimal defense strategy. Efforts to disentangle the relationship between an individual’s immune response, parasite control, and host fitness have been increasingly encouraged within the context of natural populations subject to a full range of selective pressures (Viney et al. 2005, Hawley and Altizer 2011, Pedersen and Babayan 2011). Here, we measured natural antibodies (natural IgM & IgG) and the magnitude of specific antibody titers as indices of immune responsiveness and attempted to relate these to disease risk and severity, survival, and reproduction within a wild population of gray wolves in Yellowstone National Park. Canine distemper virus and sarcoptic mange have measurable impacts on wolf pup and adult survival within our system, and we found qualified evidence that several of our indices of innate immune responsiveness significantly interacted with these pathogens to affect host mortality risk. Natural IgM and IgG levels were positively and negatively associated with survival, respectively, given infection with mange. Natural IgG was also positively associated with survival given infection with CDV. These results, however, were dependent on the inclusion of four statistical outliers; when we removed these individuals from the dataset, we no longer found evidence that natural antibodies interacted with pathogen exposure to affect survival. We found that natural IgM exhibited an age-dependent relationship with survival, suggesting that very high levels of natural IgM in young animals were associated with an increased risk of mortality. None of our immune indices explained variation in infection risk or severity. We found no evidence for a tradeoff between immune responsiveness and reproduction: a mother’s indices of immune responsiveness were unrelated to her litter size or pup survival. Intellectual merit and broader impacts Our work has attempted to bridge within-host dynamics to population-level dynamics by linking individual immune investment to survival and reproduction given pathogen exposure. Despite the fact that we found significant interactions between natural antibodies and survival given pathogen exposure, it is not clear whether natural antibodies hold widespread promise as an index for immune responsiveness. Our results were driven by several outliers; while these outliers may represent real and important variation upon which natural selection acts, they are so rare that it limits the value of these indices for predicting population-level responses to infection. Future work on similarly well-studied, wild populations may offer insights into the overall variability of natural antibodies within and across populations and their usefulness in explaining variation in response to infection. Our study has had the broader impact of expanding the training and skill sets of an outstanding female graduate student. The project has built on a rich, long-term public dataset on a wild carnivore, adding a novel component of interest to the larger ecological community. Furthermore, the results from our study will be disseminated in the form of public lectures through the National Park Service and to interested school groups. Research results will also be published on a citizen science website, developed as part of the authors’ larger disease monitoring project, that uses visiting photographers to monitor the individual-level variation in the severity of infection of wolves with sarcoptic mange. Literature Cited Graham, A. L., D. M. Shuker, L. C. Pollitt, S. Auld, A. J. Wilson, and T. J. Little. 2011. Fitness consequences of immune responses: strengthening the empirical framework for ecoimmunology. Functional Ecology 25:5-17. Hawley, D. M. and S. M. Altizer. 2011. Disease ecology meets ecological immunology: understanding the links between organismal immunity and infection dynamics in natural populations. Functional Ecology 25:48-60. Pedersen, A. B. and S. A. Babayan. 2011. Wild immunology. Molecular Ecology 20:872-880. Viney, M. E., E. M. Riley, and K. L. Buchanan. 2005. Optimal immune responses: immunocompetence revisited. Trends in Ecology & Evolution 20:665-669.
