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Abstract
Parasites are ubiquitous in natural populations, and can exert strong selection on hosts to defend themselves from infection pathology. Parasites are also often heterogeneously distributed across host habitats, in terms of pathogenicity, diversity and prevalence. The extent to which parasite infection risk constitutes a force of selection for host resource allocation to defense is expected to depend on both the likelihood of encounter and the fitness consequences of infection. Adaptation of hosts to local parasite selection regimes also depends on host gene flow between transmission hotspots and coldspots. I used two different types of marine invertebrate hosts (snails in the genus Littorina, and the shore crab Hemigrapsus sanguineus) and their common castrating parasites to test 1) whether wild hosts experiencing divergent parasite selection regimes were adapted to local levels of infection risk, and in the shore crab hosts, 2) whether hosts experiencing a reprieve from infection risk in their invasive range showed altered energy allocation to immune defenses and other fitness traits. In Littorina snails, I used a common garden experiment to test whether historical exposure to high or low castrating trematode parasite infection risk predicts the ability of snails to avoid or defend against trematode infection, and whether host local adaptation to infection is influenced by host population genetic admixture as determined by each species reproductive most. For the two Littorina host species with direct development of offspring and thus low population admixture, snails originating from high infection-risk environments were less susceptible to infection than snails from nave populations. Next, because introduced species often escape from infection risk from their co-evolved native parasites, we hypothesized that invasive host populations may respond to relaxed parasite selection in the invasive range by redistributing resources away from immune defenses and toward other fitness traits. A common garden experiment comparing infection susceptibility in H. sanguineus from the native range, where castrating rhizocephalan barnacle parasites are common, to susceptibility in invasive-range crabs where these parasites are absent showed higher susceptibility among invasive-range crabs. An exploration of immune defense traits and energy storage revealed that invasive range crabs have lower self-maintenance metabolic costs and altered relationships between reproductive energy investment and immune trait investment. In invasive species, these results support that invasive populations that experience reduced selection from the parasites with which they co-evolved may re-allocate defense resources to competing fitness traits, but that reduced defense investment comes at the cost of heightened susceptibility to infection. Overall, this dissertation supports that parasites constitute a strong force of selection acting on host resource allocation, and that the loss or intentional removal of parasites from host populations may result in host populations that are vulnerable to future infections.