WILDLIFE MICROBIAL ECOLOGY
Wildlife microbiomes, the complex communities of microorganisms that inhabit virtually every body site, perform countless micro-ecosystem services for their host, profoundly affecting wildlife behavior, physiology, reproduction, health, survival and ultimately evolution. For example, gut microbiomes metabolize compounds that their host cannot, aid in vitamin synthesis, facilitate tissue development, and contribute to myriad immune system responses, whereas skin microbiomes provide protection from pathogens and UV-radiation. These tightly co-evolved host-microbe systems also are sensitive to perturbations in the host’s environment (e.g., anthropogenic disturbance, climate change, radionuclide exposure). Plasticity in wildlife microbiome composition and community membership is an underappreciated source of adaptive potential for species coping with environmental change. The WECOS Lab seeks to (a) advance our knowledge of the eco-evolutionary factors (e.g., sex, diet, parasite load, habitat, phylogeny) governing wildlife-associated microbiomes, (b) identify species-specific microbiomes that can serve as sentinels for environmental quality and food availability, thereby providing calibration for novel tools that can serve as biomarkers for wildlife population health, (c) evaluate the impact of environmental perturbations on wildlife microbiome functions, and (d) inform management decisions to promote long-term conservation of wildlife and their symbiotic microbes.
IMPACTS OF HUMAN-PROVISION FOODS ON BLACK BEAR GUT MICROBIOMES
Many factors (e.g., phylogeny, life stage, sex) influence gut microbiome diversity and community composition in mammals, although diet has be identified as a primary driver of mammalian gut microbiome structure and function. Thus, human-mediated perturbations to natural food webs may shift and possibly decouple the tightly co-evolved relationships between mammals and their microbes with unforeseen consequences to the health of diverse species. As common carnivore that is widely distributed, has a broad diet and can be legally harvested over human-provisioned foods (i.e., bait), American black bears (Ursus americanus) are an excellent model for investigating the impact of human-mediated food web perturbations on the gut microbiome of a wild carnivore. We are studying black bear-gut microbiome relations in two populations: the Upper Peninsula of Michigan and coastal North Carolina. In the Upper Peninsula of Michigan, hunters are allowed to bait with processed foods (e.g., confectionaries, dog food), whereas in coastal North Carolina baiting is restricted to unprocessed foods (i.e., corn and peanuts). By teaming up with hunters, guides, and wildlife managers we are able to obtain samples from operationally distinct regions of the gastrointestinal tract of legally harvested bears to examine whether the impacts of human-provisioned foods differentially affect microbial communities along the gastrointestinal tract. We are subsequently using a combination of 16S rRNA sequencing (microbiome) and stable isotope analysis (diet) to examine how the proportional contribution of human-provisioned foods to the diet of black bears affect their gut microbiomes. We hope this work will serve as a catalyst for future studies to aid the effective management of healthy wild bears and their symbiotic gut microbiomes.
CAUSES AND CONSEQUENCES OF VARIATION IN BROWN BEAR GUT MICROBIOMES
As one of the most admired, enigmatic, and ecologically influential terrestrial mammals, the brown bear (Ursus arctos) is an intriguing ecological model in which to examine factors that modulate carnivore gut microbiome diversity and community membership for application to mammal conservation worldwide. First, brown bears employ diverse feeding strategies ranging from highly carnivorous to highly herbivorous, which presentes an excellent opportunity to examine the role that diet plays in structuring gut microbiome communities in a large mammal. Second, like most carnivores, the brown bear is a fast digester and rapid transit time from food consumption to feces production means there is little time for the immune system to filter and select from the diversity of environmental microbes entering the body with food. As such, the brown bear gut microbiome likely reflects habitat quality. Finally, brown bears are a species of management concern across much of their North American and Eurasian ranges and extensive research-based handling means there is an abundance of physiology/ecological (e.g., reproductive status, lean muscle mass, diet) and environmental data (e.g., elevation, human disturbance) that can be linked to fecal samples for investigating gut microbiome taxonomic diversity and community structure. Across Alaska, we will identify the drivers of variation in brown bear gut microbiomes and correlate this variation to measure of brown bear health. This initiative is a collaboration among Northern Michigan University, National Park Service, US-Geological Survey, and US-Fish and Wildlife Service.
EFFECTS OF RADIONUCLIDE EXPOSURE ON WILD BOAR GUT MICROBIOMES
While gut microbiome taxonomic diversity and community membership depends on many factors (e.g., diet, life stage, sex), the impact of environmental pollution on gut microbiomes is poorly known. Given the role that gut microbiomes play in detoxifying dietary intake for some contaminants, understanding the extent to which chronic radionuclide exposure influences gut microbiome diversity (i.e., richness, evenness, phylogenetic diversity) and function in wildlife will produce novel insights into potential sub-lethal effects of contaminant exposure. We are characterizing and quantifying taxonomic and phylogenetic diversity and exploring variation in microbial function in the gut microbiome of wild boar (Sus scrofa) exposed to varying levels of radionuclides across the Fukushima-Daiichi Nuclear Exclusion Zone. Wild boar and humans have similar diets (e.g., omnivorous) and structurally/functionally similar gastrointestinal tracts, thus our work may provide insights that relate human health. This initiative is a multi-institutional collaboration among Northern Michigan University, Fukushima University, Tokyo University of Agriculture, North Carolina State University, and University of Georgia.
BLUE-SPOTTED SALAMANDER POLYMORPHS HOST DIFFERENT SKIN MICROBIOMES
Amphibian skin, like that of all animals, hosts a consortium of microorganisms that facilitate critical micro-ecosystem services such as vitamin synthesis, parasite/pathogen defense and UV-protection. Though ecologists increasingly appreciate the role skin‐associated microbiomes play in amphibian ecology and evolution, we know surprisingly little about the specificity of microbiomes to their amphibian hosts. For example, previous studies have shown that different amphibian species inhabitating the same pond harbor unique skin microbiomes; however, we lack knowledge as to whether polymorphs inhabitating the same habitat harbor different skin microbiomes or whether skin-associated microbiome differences relate to genetic differences between polymorphs. Understanding the similarities and differences in skin microbiomes between polymorphs inhabiting the same environment is essential to understanding skin symbiont microbial community assembly, intra-population variation in disease susceptibility, and ultimately, the role skin microbiomes play in the extended host phenotype. The blue-spotted salamander (Ambystoma laterale) is a polymorphic species that is widely distributed aross much of eastern North America and provides an excellent model system in which to investigate microbiome differences between polymorphs inhabiting the same habitat. As such, we are characterizing and quantifing taxonomic and phylogentic differences in skin-microbiome diversity in a polymorphic population of blue-spotted salamanders at Presque Isle Park, Marquette, MI.
HARNESSING CITIZEN SCIENTISTS TO INVESTIGATE WATERFOWL MICROBIOMES
Phylogeny and diet influence gastrointestinal tract morphology and associated gut microbiomes that facilitate countless micro-ecosystem services critical to host health. Gut microbiomes, however, also influence gastrointestinal tract morphology and host diet. Thus, understanding these complex reciprocal relationships is critical to advancing our knowledge of the natural history of Earth’s macro and micro-biodiversity. However, for most wildlife, we know little regarding the extent to which gastrointestinal tract morphology varies among individuals within a species or how variation in gastrointestinal tract morphology relates to differences in the microbiome of the host. Using waterfowl as an exciting ecological model due to their complex gastrointestinal tract morphology (e.g., gizzard, small and large intestine, paired ceca) and our ability to opportunistically sample animals across diverse phylogenies by engaging hunters as citizen scientists, we are evaluating (a) among-individual variation in gastrointestinal tract morphology within and among different species of migratory waterfowl and (b) assessing whether variation in gastrointestinal tract morphology relates to among-individual differences in gut microbiome diversity and community membership across the gastrointestinal tract.
AMERICAN MARTEN-PARASITE-MICROBIOME INTERACTIONS
The majority of mammalian microbes live in the gastrointestinal tract of their host, and the genes and genomes of these microbes (i.e., gut microbiome) encode myriad metabolic functions critical to mammalian ecology and evolution. Although the vast majority of host-microbiome studies focus on humans or model organisms in laboratory settings, these studies provide conceptually rich evidence that disruption of the host-gut microbiome relationship (i.e., dysbosis) can negatively affect host health, fitness and survival. However, among the many factors that can induce dysbiosis in wildlife (e.g., psychological stress, food stress), parasitic infections represent a potentially potent, yet poorly understood factor that may affect gut microbiome diversity, community structure and function. Using American marten (Martes americana) as a model species, we are examining host-parasite-microbiome interactions to learn how aspects of disease ecology can be integrated into wildlife studies to advance conservation science and practice. To achieve this goal, we are collaborating with Alaska Department of Fish and Game to opportunistically acquire marten gastrointestinal tracts from legally harvested animals donated by trappers in Alaska and with the Northern Michigan University Vertebrate Zoology Museum. Given the unprecedented rates of disease emergence, a better understanding of host-parasite-microbiome interactions may illuminate novel opportunities to mitigate conservation disasters and public health crises.
