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Tritrophic Consequences of Host Range Expansion: The Impacts of Exotic Host Plants on Infection and Immunity in Native Insect Herbivores
AuthorMuchoney, Nadya Dougherty
AdvisorSmilanich, Angela M
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Species introductions are a pervasive aspect of global change. Exotic plants, in particular, are present in nearly all terrestrial environments and have been incorporated into the diets of many native herbivores, giving rise to novel multitrophic interactions. These recent examples of host range evolution provide naturally occurring experiments through which to investigate the complex ecological factors that facilitate, or constrain, herbivore persistence within novel niches. Though adoption of exotic plants into the diets of native insect herbivores is common, their use is often associated with negative effects on herbivore growth and performance, relative to native host plants. However, herbivore fitness on different host plants is context-dependent and shaped by a multitude of factors beyond suitability for development, including interactions with diverse natural enemies. Consideration of herbivore performance within a tritrophic framework, including attack by and defense against these enemies, may be essential for understanding the outcomes of dietary expansion for native herbivores. In particular, entomopathogens represent critical agents of mortality for insect herbivores, yet their ecological impacts and importance in mediating diet breadth evolution remain poorly understood in many natural systems.In this dissertation, I combined approaches from the fields of eco-immunology, chemical ecology, and disease ecology to investigate the consequences of exotic host plant use for immune performance, chemical defense (i.e., phytochemical sequestration), and vulnerability to a viral pathogen in two North American herbivores: Euphydryas phaeton, the Baltimore checkerspot (Lepidoptera: Nymphalidae), and Anartia jatrophae, the white peacock (Lepidoptera: Nymphalidae). These herbivores provide compelling systems in which to compare the tritrophic outcomes of host range expansion, as they: (1) recently incorporated the same exotic plant, Plantago lanceolata (Plantaginaceae), into their diets, (2) exhibit reduced growth on the exotic plant, relative to native host plants, (3) are infected by the same entomopathogen, Junonia coenia densovirus, across wild populations, and (4) differ in their degree of dietary specialization and relationships with plant secondary chemistry, which can impact immunity and susceptibility to pathogens. Employing a combination of field-based surveys and manipulative laboratory experiments, I found that the outcomes of dietary expansion for herbivore infection and immunity differed across the two focal species. In E. phaeton, use of the exotic plant was associated with suppression of multiple immune parameters, differential sequestration of defensive phytochemicals (iridoid glycosides), and higher viral burdens during certain stages of development, representing potential costs of host range expansion. However, E. phaeton’s ability to survive densovirus infection was not reduced on the exotic host plant, suggesting that additional factors (e.g., phytochemical sequestration) may contribute to defense against this pathogen even when immunity is compromised. In contrast, use of the exotic plant dramatically increased resistance to viral infection in A. jatrophae, likely through suppression of replication, though immune performance did not vary based on host plant use. Together, this research demonstrates that, in certain systems, exotic host plants may represent equally suitable or even superior resources for supporting herbivore development, relative to native host plants, when the impacts of pathogen infection are considered. Moving forward, evaluation of the role of host plant use in mediating defense against infectious diseases across wild populations may provide a deeper understanding of the complex ecological factors shaping host range evolution in herbivorous species.