Variable immunity and its consequences for parasite dynamics

Infectious disease represents a growing concern for our developing world. Human diseases result in morbidity, mortality, and suffering. Agricultural diseases can decimate food resources, leading to starvation and economic instability. Wildlife diseases affect the abundance and distribution of species, destabilizing the natural ecosystems on which we rely. Despite these varied contexts, infectious diseases can be united by three common factors: susceptible hosts, parasites, and environmental conditions. Over the past three decades, disease ecology has provided overwhelming evidence that environmental conditions can shape disease risk by altering host-parasite interactions. For example, shifting global temperatures can increase the density of pathogen vectors, thereby increasing pathogen transmission to humans. Such work has long relied on simple mass action principles of transmission, where infections are driven by rates of exposure and hosts are ascribed a single value denoting their susceptibility to infection. However, accumulating evidence suggests that this single value is biologically unrealistic, with most organisms exhibiting considerable variation in their natural levels of susceptibility. Moreover, theoretical models predict that variation in susceptibility can have profound consequences for the spread of disease. Connecting variable susceptibility to its epidemiological outcomes has become an emerging goal in ecology which I have addressed using observation, modeling, and experiments. At the heart of host susceptibility is the immune response. All living organisms are threatened with parasites and, in turn, utilize a suite of immunological defenses to prevent infection. Because immune defenses are important for defeating infections at the individual level, they may also present a barrier to disease transmission at the population level. I have investigated immune defenses and their consequences for parasites in an aquatic host-parasite system: the zooplanktonic host Daphnia dentifera and its fungal pathogen Metschnikowia bicuspidata. In my first chapter, I describe the complete life cycle of Metschnikowia, detail its within-host interactions with Daphnia, and outline the potential defenses Daphnia use to prevent infection. Through Chapter one, I overturned a longstanding assumption that Daphnia cannot recover from infection and developed a series of metrics for quantifying components of the host-parasite interaction. These empirical metrics are specific to the Daphnia-Metschnikowia system, and in my second chapter, I developed a mechanistic modeling approach for estimating host immune defenses that can be applied across wildlife systems. Working closely with Dr. Zoi Rapti, I developed a discrete-state continuous-time Markov model to estimate the probabilities with which organisms resist and clear parasitic infections. In Chapter 3, I quantified the relative importance of Daphnia susceptibility for the emergence of Metschnikowia epidemics. From pre- to peak- epidemic periods, I tracked Metschnikowia exposure and Daphnia recovery rates in six lake ecosystems and found that epidemic emergence depends critically on the interaction between parasite exposure and host susceptibility. In my fourth and final chapter, I tested several hypotheses regarding the nature of Daphnia susceptibility and identified which host traits are the most critical for determining the outcome of infection. Together, my dissertation provides a comprehensive set of empirical studies demonstrating how exposure and susceptibility interact to regulate parasites and the spread of disease in wildlife.

Name thesis:degree_name

Ph.D.

Level thesis:degree_level

Dissertation

Discipline thesis:degree_discipline

Ecol, Evol, Conservation Biol

Grantor

University of Illinois at Urbana-Champaign

Year dc:date

2019

Author dc:creator

• Stewart Merrill, Tara E.

Contributors dc:contributor

• Cáceres, Carla E
• Allan, Brian F
• Fuller, Rebecca C
• O'Dwyer, James P
• Rapti, Zoi

• Susceptibility
• immunity
• disease
• parasite
• transmission
• ecological immunology
• invertebrate immunology
• Daphnia
• Metschnikowia
• epidemic
• Markov model

Statement dc:rights

• Copyright 2019 Tara E Stewart Merrill

Language dc:language

en

Handle dc:identifier

http://hdl.handle.net/2142/105796

OAI identifier oai:identifier

oai:www.ideals.illinois.edu:2142/105796