Ecological and evolutionary sources of variation in immune phenotype, in theory and in practice

Abstract

Organisms employ a great variety of immune defenses to counter parasites, and immune strategies can differ substantially among and within populations. As yet, however, the factors structuring that variation are poorly-understood. Immune defenses are costly to produce, and they pose their own risks to the host through immunopathology. Parasite risk variation does drive variation in immune phenotypes, but a myriad other factors play significant roles as well. Among the most notable is life history, which shapes demographies and the allocation of resources to different functions, including immunity; social context, diet, and even climate can also drive immune variation. In this thesis, I explore how to assess immune variation, how it is structured within populations, and the role of life histories in producing different immune phenotypes. I employ several different approaches: mathematical modeling, experiments with rewilded laboratory mice, and a wild marine mammal. Chapter 1 shows that classic genotype-by-environment interactions contribute significantly to immune variation in laboratory and rewilded mice. In Chapter 2, we use behavioral ecology and social network approaches to show that mice that are more socially-associated have more similar immune phenotypes. Chapter 3 explores techniques for describing immune variation in wild animals by testing whether simple, widely-employable immune measures can be effective proxies for difficult-to-measure aspects of lymphocyte composition. Chapters 4 and 5 focus on the influence of life history on immune defenses. In Chapter 4, we use a demographic framework and model of immune specificity to show that life histories and epidemiological variation interact to shape optimal immune strategies. And Chapter 5 uses northern elephant seals (Mirounga angustirostris), a species with strong sexual selection, to examine the hypothesis that sexual selection should produce sexual dimorphism in immune phenotypes. We document sexual dimorphism in proinflammatory immune gene expression and interactive effects of age and sex on immune responses. Overall, my thesis uses evolutionary and ecological approaches to explore the nature of immune variation. We demonstrate that ecology is important for variation in immune defense and that immune phenotypes are as much an element of overall organismal strategy as any other trait.