Concomitant natural and sexual selection reveals context-dependent evolution of host resistance to parasites

Where parasites evolve to exploit, hosts evolve to resist. In nature, such coevolutionary dynamics play out in an environment with multiple concurrent selection pressures. This thesis describes the evolutionary benefit of evolved adaptive resistance to parasites and explores experimentally whether resistance can be maintained in spite of competing selective agents. Using three-spined stickleback as a model organism, I, together with colleagues, first demonstrate that under strong parasite-mediated selection the evolution of acquired immunity provides a significant reproductive advantage (Chapter 1). Next, I evaluate how predation impacts host-parasite dynamics, with a special focus on host resistance associated with polymorphism of genes of the major histocompatibility complex (MHC). I show that predation weakens parasite-mediated selection and in the process disrupts negative-frequency dependent selection on MHC haplotypes across generations (Chapter 2). Furthermore, predation can interfere with MHC-based mate choice behaviour (Chapter 3). Expanding on the evidence of context-dependent resistance to parasites, I describe how the link between parasites and specific MHC haplotypes differs seasonally and in accordance with the strength of parasite–mediated selection (Chapter 4). In the last chapter, I experimentally assemble populations with and without MHC haplotypes associated with resistance and observe whether sexual selection differs between the populations. As expected, individuals with resistance-assocaited MHC haplotypes experienced reduced burden of a specific parasite and, as consequence, increased individual lifetime reproductive success (Chapter 5). Collectively, these results underscore the importance of evolved parasite resistance for individual fitness in general. Our findings show just how context-dependent the evolution of resistance can be, with seasonal variation, concomitant predation or different strengths of sexual selection, all affecting the outcome of parasite-mediated selection and selection on immune genes. This work sheds light on why variation in the capacity to resist parasite infection exists among populations within a species or between species