I am a wildlife ecologist with training in zoology and veterinary medicine, conducting research at the intersection of disease ecology, immunological ecology, and physiological ecology. I examine infectious disease dynamics at molecular, cellular, organismal, and population levels, with the primary goal of understanding host-pathogen interactions. As a veterinarian, I possess a deep understanding of the physiological, immunological, and pathological processes involved in a host’s response to disease. As a zoologist and ecologist with veterinary training, I am thus in the unique position of being able to examine disease processes in natural systems from the point of view of internal host dynamics, and to conduct comprehensive immunological studies in wildlife. By studying environmentally transmitted diseases, my work also bridges the gap between internal host ecosystems and the external environment. Overall, I strive to understand why hosts get the diseases they do, when they do. To this end, my research involves three main, complementary themes:
1. Host susceptibility to disease, and how susceptibility and disease dynamics fluctuate seasonally
2. Within-host coinfection and immune trade offs
3. Examining hosts as internal ecosystems
1. Seasonally Driven Host Susceptibility to Disease
I am interested in what makes one host more susceptible to disease than another host in its population. Expanding this to the population level, I am interested in why populations of hosts experience disease outbreaks contained in space and time. I address these issues by examining host physiological and immunological traits in concert with markers of infection, comparing these measures temporally. My doctoral dissertation research focused on how host susceptibility to anthrax changed seasonally in Etosha National Park, Namibia, a natural, uncontrolled anthrax system in which plains ungulates experience annual, wet season anthrax outbreaks. Given the facts that anthrax can only be transmitted (usually orally) environmentally and that the bacteria exist in the environment as hardy, very long-lived spores that do not appear to undergo appreciable environmental replication, it is unclear why natural anthrax outbreaks occur rather than a more constant incidence of this disease. For this work, I examined seasonal differences in host immune allocation, both generally (likely due to changes in resource abundance) and in association with seasonally-constrained, directly transmitted gastrointestinal (GI) parasites, hormonal changes, and anthrax exposure.
As part of my postdoctoral research at Princeton University, I am again studying the seasonality of environmentally transmitted pathogens, focusing primarily on GI parasites in non-human primates in Laikipia Province, Kenya. I am examining host gut immune factors in concert with seasonal fluctuations in GI parasite infection intensity and composition, particularly looking at how gut IgA antibody titers vary with season and infection. In addition, I am examining the host gut microbiome in concert with seasonal parasite infection intensity fluctuation. In addition, I am a founding member of a multi-institution Parasite Ecology Research Project (PERP) examining the effects of climate change on parasite biodiversity and vulnerability to extinction. By building models using new theories and existing datasets, we are examining how parasites, particularly environmentally transmitted pathogens, may be affected by different climate change scenarios, including how increased seasonal fluctuations or seasonal damping may affect host-pathogen dynamics.
2. Within-Host Coinfection and Immune Trade-Offs
Macroparasites, in particular GI helminths, have been found in many laboratory studies to be immunomodulatory in hosts. These large worms typically skew host immune function toward the Th2-type arm of immunity, which is ineffective in fighting against most microparasite infections (most intracellular bacteria and viruses). Microparasite infections largely require a Th1-type immune response from the host for control and clearance of infection, and these two immune arms are usually mutually exclusive and mutually inhibitory. While these patterns have been demonstrated in many laboratory systems, they have only been shown in a couple of studies in complex natural systems. For my dissertation research, I found strong evidence that GI parasites skew zebra hosts toward a Th2-type immune response during the wet season, and that this likely contributes to making these hosts more susceptible to fulminant anthrax infection at this time. In addition, I found that GI parasite immunomodulation also correlates with increased host susceptibility to ectoparasite infestations, illustrating that GI parasites are likely the primary drivers of host immunomodulation in this system. While I expected these GI parasite infections in turn to increase host stress in the wet season, I found that stress hormone levels were in no way correlated with GI parasite infection intensities, indicating that these hosts are largely tolerant of their macroparasites despite the number of resources they command.
I am continuing to examine issues of immune trade offs, coinfection trade offs, and tolerance and resistance in my postdoctoral work. While my study animals in Etosha were infected with only one or two species of gut macroparasites, my study primates in Kenya experience more diverse macroparasite coinfections. Thus, I am examining the hierarchy of host immunomodulation and immune resource usage by the different GI parasites in these hosts: i.e. Which parasites command host resistance resources (such as parasite-specific IgA)? Which parasites are the hosts largely tolerant of? Which parasites affect the host microbiome the most? Which parasites drive infection transmission dynamics between troops? In addition, the PERP group is examining how parasite coinfection dynamics may change under different climate change scenarios, as some parasite species thrive and outcompete others, and as host-parasite mismatch occurs.
3. Hosts as Internal Ecosystems
The discipline of ecological immunology is still in its infancy; the majority of immunological studies in wildlife to date have measured just one or two basic components of host immunity and host-pathogen interactions. While examining immune function in natural settings is complex due to individual variation, seasonal fluctuations, and innumerable other factors that must be controlled for, I feel strongly that we must ultimately ground-truth the findings from highly controlled laboratory studies in natural systems. Thus, for my dissertation research, I measured nine measures of immune function, four hormones, several body measurements, infection with three pathogens, and several environmental parameters in my study animals. In addition, I performed the first longitudinal, comprehensive ecological immunology study in the wild, as I resampled my study animals as many times as possible over five seasons to control for individual variation and to examine pathogen and immune changes over time. While I have used these data to examine several hypotheses thus far (see above), I am also interested in quantifying the relationships between all components within these hosts. I am currently working on developing an internal host “food web” using path and cluster analyses; while a few other studies have attempted to quantify the internal host ecosystem, the wealth of data I possess for each of my study animals over time will allow me to create the most comprehensive analysis of internal host ecosystems to date. While this is a valuable exercise in and of itself to both highlight the complexity of the internal host milieu and to drive the further development of these methods, such networks will also help to elucidate complex host-pathogen interactions from a within-host perspective and will help drive future research efforts.
I will also build within-host ecosystem networks for my current primate work; although I will, at present, be unable to do animal captures and obtain blood from these animals, limiting me to gut host and pathogen measurements, the addition of the host microbiome as a further nested ecosystem will allow me to examine within-host complexity in an entirely new way. In addition, I plan to determine the gut microbiota components of my previously examined zebra by using banked fecal samples. When I have this data, I will include this nested ecosystem within my zebra “internal food webs.” Again, these interactions will help to elucidate new and complex patterns, and will help to drive future work.