High-Throughput Sequencing for Understanding the Ecology of Emerging Infectious Diseases at the Wildlife-Human Interface

Rising rates of emerging infectious diseases (EIDs) demand creative, efficient, and integrative investigations to understand their transmission, ecological contingencies, and dynamics at wildlife-human interfaces. High-throughput sequencing (HTS) methodologies provide enormous potential to unravel these contingencies to improve our understanding, but their potential is only just starting to be realized. While recent work has largely focused on novel pathogen discovery at likely interfaces, high-throughput methods can also allow disease ecologists to better explore the critical effects of climate, seasonality, and land-use changes on EIDs. HTS can facilitate the creation of entire host-pathogen networks, integrate important microbiome and co-infection data, and even pinpoint important exposure routes at interfaces through environmental media. Here we highlight studies at the frontier of HTS and disease ecology research, identify current limitations, and outline promising future applications for EIDs

More than mimicry? Evaluating scope for flicker-fusion as a defensive strategy in coral snake mimics

Coral snakes and their mimics often have brightly colored banded patterns, generally associated with warning coloration or mimicry. However, such color patterns have also been hypothesized to aid snakes in escaping predators through a “flicker-fusion” effect. According to this hypothesis, banded color patterns confuse potential predators when a snake transitions from resting to moving because its bands blur together to form a different color. To produce this motion blur, a moving snake’s bands must transition faster than the critical flicker-fusion rate at which a predator’s photoreceptors can refresh. It is unknown if coral snakes or their mimics meet this requirement. We tested this hypothesis by measuring the movement speed and color patterns of two coral snake mimics, Lampropeltis triangulum campbelli and L. elapsoides, and comparing the frequency of color transitions to the photoreceptor activity of the avian eye. We found that snakes often produced a motion blur, but moving snakes created a blurring effect more often in darker conditions, such as sunrise, sunset, and nighttime when these snakes are often active. Thus, at least two species of coral snake mimics are capable of achieving flicker-fiision, indicating that their color patterns may confer an additional defense aside from mimicry

Large-herbivore nemabiomes: patterns of parasite diversity and sharing

Amidst global shifts in the distribution and abundance of wildlife and livestock, we have only a rudimentary understanding of ungulate parasite communities and parasite-sharing patterns. We used qPCR and DNA metabarcoding of fecal samples to characterize gastrointestinal nematode (Strongylida) community composition and sharing among 17 sympatric species of wild and domestic large mammalian herbivore in central Kenya. We tested a suite of hypothesis-driven predictions about the role of host traits and phylogenetic relatedness in describing parasite infections. Host species identity explained 27 – 53% of individual variation in parasite prevalence, richness, community composition and phylogenetic diversity. Host and parasite phylogenies were congruent, host gut morphology predicted parasite community composition and prevalence, and hosts with low evolutionary distinctiveness were centrally positioned in the parasite- sharing network. We found no evidence that host body size, social-group size or feeding height were correlated with parasite composition. Our results highlight the interwoven evolutionary and ecological histories of large herbivores and their gastrointestinal nematodes and suggest that host identity, phylogeny and gut architecture — a phylogenetically conserved trait related to parasite habitat — are the overriding influences on parasite communities. These findings have implications for wildlife management and conservation as wild herbivores are increasingly replaced by livestock

The Role of Watering Holes as Hotspots of Disease Transmission in Changing Climates

Humans impact the globe in numerous ways that have important yet variable effects on human and animal diseases. Anthropogenic changes may be particularly consequential where landscape resources increase transmission opportunities; however, these spatial hotspots of human and animal activity are a relatively understudied aspect of disease dynamics. Watering holes are an ideal system for studying such transmission hotspots amid accelerating global changes, as they draw together wildlife, domestic animals, and humans in arid climates that are increasingly impacted by climate change. In this dissertation, I used observational and experimental data to investigate plants, herbivores, and gastrointestinal parasites at these important ecological resources in a semi-arid savanna system in central Kenya. I first examined how watering holes and associated herbivore aggregations shape plant communities that form the transmission substrate for many fecal-oral parasites. I found that herbivore aggregation near water was associated with decreased plant cover but opposing plant diversity patterns, depending on soil and rainfall. This was driven by changes in grass and tree cover and dominance shifts of two globally important grass species. I then used a two-year water manipulation experiment and observational study to examine the extent to which herbivores and their gastrointestinal parasites aggregated near water sources under different gradients of water availability: aridity, recent rainfall, and distance from surface water. I found marked differences in dung and parasite aggregation at water by herbivore species, with elephants and cattle congregating strongly in arid conditions. However, all animals displayed some degree of increased watering hole use with at least one metric of decreased water availability, suggesting that drying environments may contribute to increased parasite concentration at these hotspots across species. I then investigated gastrointestinal parasite communities in 18 sympatric and globally threatened herbivore species using DNA metabarcoding I found that host phylogeny and gut type were central in determining parasitic nematode sharing. I linked data on parasite spatial aggregation and sharing to data from an 8000-volunteer citizen science project measuring herbivore activity from camera traps to estimate parasite transmission near water relative to dry sites. I found that due to their abundance, degree of aggregation around water, and ability to share parasites, cattle were strong potential drivers of gastrointestinal parasite transmission for other herbivore species at watering holes. Together, these findings demonstrate predictable patterns of parasite transmission in resource-limited areas and have implications for understanding and predicting disease dynamics in humans, wildlife, and domesticated animals that live in increasingly dry landscapes

Interacting effects of wildlife loss and climate on ticks and tick-borne disease

Understanding the effects of anthropogenic disturbance on zoonotic disease risk is both a critical conservation objective and a public health priority. Here, we evaluate the effects of multiple forms of anthropogenic disturbance across a precipitation gradient on the abundance of pathogen-infected small mammal hosts in a multi-host, multi-pathogen system in central Kenya. Our results suggest that conversion to cropland and wildlife loss alone drive systematic increases in rodent-borne pathogen prevalence, but that pastoral conversion has no such systematic effects. The effects are most likely explained both by changes in total small mammal abundance, and by changes in relative abundance of a few high-competence species, although changes in vector assemblages may also be involved. Several pathogens responded to interactions between disturbance type and climatic conditions, suggesting the potential for synergistic effects of anthropogenic disturbance and climate change on the distribution of disease risk. Overall, these results indicate that conservation can be an effective tool for reducing abundance of rodent-borne pathogens in some contexts (e.g. wildlife loss alone); however, given the strong variation in effects across disturbance types, pathogen taxa and environmental conditions, the use of conservation as public health interventions will need to be carefully tailored to specific pathogens and human contexts. This article is part of the themed issue ‘Conservation, biodiversity and infectious disease: scientific evidence and policy implications’

Interacting effects of wildlife loss and climate on ticks and tick-borne disease

Understanding the effects of anthropogenic disturbance on zoonotic disease risk is both a critical conservation objective and a public health priority. Here, we evaluate the effects of multiple forms of anthropogenic disturbance across a precipitation gradient on the abundance of pathogen-infected small mammal hosts in a multi-host, multi-pathogen system in central Kenya. Our results suggest that conversion to cropland and wildlife loss alone drive systematic increases in rodent-borne pathogen prevalence, but that pastoral conversion has no such systematic effects. The effects are most likely explained both by changes in total small mammal abundance, and by changes in relative abundance of a few high-competence species, although changes in vector assemblages may also be involved. Several pathogens responded to interactions between disturbance type and climatic conditions, suggesting the potential for synergistic effects of anthropogenic disturbance and climate change on the distribution of disease risk. Overall, these results indicate that conservation can be an effective tool for reducing abundance of rodent-borne pathogens in some contexts (e.g. wildlife loss alone); however, given the strong variation in effects across disturbance types, pathogen taxa and environmental conditions, the use of conservation as public health interventions will need to be carefully tailored to specific pathogens and human contexts. This article is part of the themed issue ‘Conservation, biodiversity and infectious disease: scientific evidence and policy implications’

Interacting effects of wildlife loss and climate on ticks and tick-borne disease

Understanding the effects of anthropogenic disturbance on zoonotic disease risk is both a critical conservation objective and a public health priority. Here, we evaluate the effects of multiple forms of anthropogenic disturbance across a precipitation gradient on the abundance of pathogen-infected small mammal hosts in a multi-host, multi-pathogen system in central Kenya. Our results suggest that conversion to cropland and wildlife loss alone drive systematic increases in rodent-borne pathogen prevalence, but that pastoral conversion has no such systematic effects. The effects are most likely explained both by changes in total small mammal abundance, and by changes in relative abundance of a few high-competence species, although changes in vector assemblages may also be involved. Several pathogens responded to interactions between disturbance type and climatic conditions, suggesting the potential for synergistic effects of anthropogenic disturbance and climate change on the distribution of disease risk. Overall, these results indicate that conservation can be an effective tool for reducing abundance of rodent-borne pathogens in some contexts (e.g. wildlife loss alone); however, given the strong variation in effects across disturbance types, pathogen taxa and environmental conditions, the use of conservation as public health interventions will need to be carefully tailored to specific pathogens and human contexts. This article is part of the themed issue ‘Conservation, biodiversity and infectious disease: scientific evidence and policy implications’

Data from: Interacting effects of wildlife loss and climate on ticks and tick-borne disease

Both large-wildlife loss and climatic changes can independently influence the prevalence and distribution of zoonotic disease. Given growing evidence that wildlife loss often has stronger community-level effects in low-productivity areas, we hypothesized that these perturbations would have interactive effects on disease risk. We experimentally tested this hypothesis by measuring tick abundance and the prevalence of tick-borne pathogens (Coxiella burnetii and Rickettsia spp.) within long-term, size-selective, large-herbivore exclosures replicated across a precipitation gradient in East Africa. Total wildlife exclusion increased total tick abundance by 130% (mesic sites) to 225% (dry, low-productivity sites), demonstrating a significant interaction of defaunation and aridity on tick abundance. When differing degrees of exclusion were tested for a subset of months, total tick abundance increased from 170% (only mega-herbivores excluded) to 360% (all large wildlife excluded). Wildlife exclusion differentially affected the abundance of the three dominant tick species, and this effect varied strongly over time, likely due to differences among species in their host associations, seasonality, and other ecological characteristics. Pathogen prevalence did not differ across wildlife exclusion treatments, rainfall levels, or tick species, suggesting that exposure risk will respond to defaunation and climate change in proportion to total tick abundance. These findings demonstrate interacting effects of defaunation and aridity that increase disease risk, and they highlight the need to incorporate ecological context when predicting effects of wildlife loss on zoonotic disease dynamics