Vector-borne and zoonotic diseases (e.g. Lyme Disease, West Nile virus) have become an increased public health and wildlife management concern in the US and globally. Recent research in disease ecology has greatly improved our understanding of the behavior and dynamics of parasites and pathogens. While evidence shows some hosts become infected or transmit pathogens more than others, most theoretical models describing disease dynamics have ignored differences among individuals. Sources of individual variability such as sex, age, pathogen co-infection status, previous infection, and immune function influence how hosts become infected. Integrating population- and individual-level approaches can better describe how pathogens are affected by the small-scale environment of the host and the larger-scale community of hosts, vectors, and pathogens, leading to better assessment of disease risk and pathogen prevalence. This research addresses the following questions: 1) How does variation among individual hosts affect parasite load and probability of infection? 2) How does variation in the probability of host infection determine pathogen prevalence at the population and community level? To address these questions, ticks and small mammal hosts will be repeatedly sampled across the season of peak tick activity, and the co-infection status of hosts and ticks, as well as the host immune response, will be evaluated. Next-generation, high throughput sequencing will be used to analyze tick and host microbial co-infection patterns. A combination of a general, functional immune assay and detailed measurement of host cytokine profiles will be used to inform how the immune system interacts with vectors and vector-borne infection.
This project investigates many levels of diversity, from bacterial to vector, host, and environment, using techniques from multiple fields of biological science. The results of this research project may lead to better on the ground assessment of human risk for vector-borne disease. The interdisciplinary nature of this research provides many opportunities for undergraduate research projects, from animal behavior to vector and pathogen genetics, making this project exciting to a broad diversity of students. Educational literature on tick-borne disease and minimizing risk will be designed for local DNR, parks and recreation groups.
Intellectual Merit One of the main challenges in studying disease in natural systems is to understand why hosts vary in how many parasites they carry, how many they transmit to others, and what impact this has on disease dynamics and host health. The aims of this project were to study how differences within and between species affect how many hosts are infected in the community. Specifically, my research questions were: 1) How does variation between individual hosts affect parasite load and probability of infection?, 2) How does variation in the probability of host infection determine pathogen prevalence (proportion of infected hosts) at the population and community level? I studied wild rodents (white-footed mice and prairie voles) and tick vectors (American dog tick, lonestar tick, and the blacklegged deer tick) to address these questions. I used mark-recapture methods to gather data on individual rodent hosts and the ticks they carried over time. I then used powerful new sequencing methods to characterize the microbial communities within the ticks and rodent blood to assess infection with tick-borne bacterial pathogens and multiple immune assays, including one never used before in wild rodents, to investigate if microbial interactions or host immune response influenced tick burden and vector-borne infection. This integration of population- and individual-level approaches provided an improved framework to evaluate how pathogens are affected by the small-scale environment of the host or vector and the larger-scale community of hosts, vectors and pathogens. I found that there was significant variation in how many ticks hosts carried, with most hosts carrying few or no ticks while a minority of hosts carried many ticks. Hosts with high tick burden also continued to have high tick burden throughout the season. This may lead to some hosts having a greater influence on maintaining ticks and tick-borne pathogens in an area. The bacterial communities were significantly different between tick species and host blood. Tick microbial communities were dominated by their species-specific endosymbionts and host blood was dominated by a common flea-borne pathogen (Bartonella). This bacteria was also found in ticks but it is unknown if ticks are also a vector. Well known pathogenic tick-borne bacteria were not common components of the tick and host microbiomes sampled here. Mice had higher innate immunity than voles as well as higher average tick burdens. Within mice, hosts with higher tick burdens had lower innate immunity along with higher levels of IL-4, a pro-inflammatory cytokine (immune signalling molecule). Adult male mice, that often carry higher tick burdens, also had higher pro-inflammatory cytokines. This variation in immune measures may help identify which hosts are likely to carry high tick burdens. Many emerging diseases are zoonotic (e.g. H1N1 flu, Lyme disease, Malaria). The better we understand the mechanisms determining parasite prevalence in a host community or population and how parasite and pathogen vector abundance changes over time and between habitats, the better we can predict outbreaks and inform the public and medical professionals. What causes hosts and vectors to carry unequal parasite or vector burdens is often not known. My research investigated mechanisms determining why some hosts are more parasitized, including host immunity and microbial interactions within host or vector. The development of new, powerful molecular and immunological tools facilitates their application to other systems that are of interest for wildlife and zoonotic diseases. Broader Impacts This research project used novel tools and approaches to better understand the tick-borne disease communities in the lower Midwest, an area with overlapping ranges of three tick species. My results have been presented to adults and children at multiple events in the Bloomington, IN community. The goal was to teach people about the ecology of ticks in the area, how pathogens are transmitted, and what we know about infection rates of ticks and how host communities influence infection risk. The interdisciplinary nature of this work has facilitated collaboration between researchers in ecology, eco-immunology, microbiology and bioinformatics, within Indiana University as well as between universities in the US and abroad.