Ecological and Evolutionary Drivers of Host Defenses and Pathogen Infectivity Shape Host-Parasite Interactions at Multiple Levels of Biological Organization

Abstract

To be classified as a parasite, a symbiont must reduce the fitness of its host (Zelmer 1998; Sorci and Garnier 2008; Méthot and Alizon 2014); as such, as a common and highly antagonistic interaction, parasitism plays an important role in shaping ecological communities and mediating host evolution. My dissertation considers various factors that modulate host and parasite fitness, including host resistance evolution, immune waning and immune escape, and ecological interactions among different parasite species. I employed two host-parasite study systems in my dissertation research: Chapters 2 - 4 use the Daphnia-microparasite study system (Daphnia is a genus of zooplankton commonly used in ecological and evolutionary research due to their experimental tractability and ecological importance in freshwater ecosystems). For Chapter 5 I use public health data on SARS-CoV-2 dynamics in the people of Southeastern Michigan. In Chapter 2 I used the Daphnia-microparasite system to review how predation, competition, and abiotic factors impact rapid host-parasite evolution. Chapter 3 addresses the impacts of sexual recombination and gene flow on the maintenance of host resistance in a cyclical parthenogen. We sampled two wild populations of Daphnia before and after sex and gene flow, then used molecular methods to genotype each animal captured; we also found the resistance phenotype of each animal by raising maternal lines and conducting experimental parasite exposures. In one population, we found that genetic diversity and resistance to infection significantly increased after sexual recombination and remained high after temporal gene flow. The second population started with high genetic diversity and high resistance and maintained these levels through recombination and gene flow. This occurred despite resistance having a fitness cost, which implicates other selective forces at work which are maintaining both high resistance and high genetic diversity. In Chapter 4 I disentangle how the density of two co-existing environmentally transmitted parasites impacts disease dynamics within individual hosts and at the scale of host populations. I found evidence of density-dependent interspecific and intraspecific impacts on parasite infectivity. I additionally found that infection class had significant impacts on host lifespan and parasite transmission. Using this data for modeling epidemics revealed that parasite dose determines the equilibrium condition of disease dynamics in this system, and that interspecific parasite-parasite interactions maintain a higher parasite burden overall. For Chapter 5 I used SARS-CoV-2 data collected from the people of Southeastern Michigan to model the joint impacts of waning host immunity and evolving SARS-CoV-2 immune escape on COVID-19 dynamics. This model has proven to be conceptually sound and will be used to predict Winter 2022-23 COVID-19 burden and explore counterfactuals around vaccine uptake and variant emergence. Overall, my research shows that host resistance (Ch 3) and immunity (Ch 5) to infection can change rapidly, and disease outbreaks can be difficult to predict as a result. This dissertation also shows that evolution of hosts (Ch 3) or parasites (Ch 5) can dampen or amplify disease prevalence. Finally, this work underscores how studying interactions between species--whether those are host-parasite or parasite-parasite interactions--requires careful consideration of parasite dose (Ch 4) and integration of fitness measures across multiple levels of biological organization (Ch 2, Ch 4).