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Craft, M. E.

Publications and source records attributed to Craft, M. E..

12 recordsLinked to original sources

Widespread occurrence of bovine-like and new viruses in wild deer across the United States

Over the past several decades, deer populations in North America have grown considerably, resulting in frequent contact with humans and livestock, and increased potential for pathogen spillover. Despite the importance of pathogen spillover among humans, wildlife, and livestock, the diversity of viruses present in deer remains largely unknown. Using a metagenomic high-throughput sequencing approach, we characterized viral communities in the upper respiratory tracts of live mule deer (Odocoileus hemionus) and white-tailed deer (Odocoileus virginianus) captured at fourteen study sites in nine states across the United States. We identified vertebrate-infecting viruses in both deer species at all but two of the study sites, located in Illinois and Utah. Viral richness did not vary among species or study sites. However, viral community composition was different across study sites but not among deer species. Amongst the detected viral sequences, several originate from or were closely related to viruses previously described in humans (e.g., severe acute respiratory syndrome coronavirus 2) and livestock (e.g., bovine-like coronavirus). We also documented viruses recently discovered in deer, such as CHeRI orbivirus 1. Finally, we identified several new putative viruses in the Picornaviridae, Rhabdoviridae and Tobaniviridae families, including a novel Aphthovirus related to bovine rhinitis A virus in both deer species, across seven states and nine study sites. Our findings expand the understanding of viral diversity in two deer species across the United States, providing important insights for managing pathogens at the wildlife, livestock, and human interface.

microbiology↗

Age-dependent effects of infection on survival of a wild rodent reservoir host

Due to long co-evolutionary histories, many zoonotic pathogens are thought to exert little or no negative effects on their wildlife reservoir hosts. However, there remains a lack of rigorous investigations in natural settings. We conducted a 3-year factorial field experiment to investigate how survival of the Puumala hantavirus (PUUV) reservoir, the bank vole, is impacted by PUUV infection, nematode infections, and food availability. We hypothesized that PUUV would not impact survival, but that coinfection with nematodes would negatively impact survival, and that increased food availability would mitigate the negative effects of coinfection. Surprisingly, we demonstrated that PUUV infected voles had substantially reduced survival when compared to uninfected voles, and this strong negative effect manifested in young voles. Nematode removal increased survival of young voles and food supplementation interacted with movement rather than survival. Our results provide empirical evidence in a natural system for infection reducing survival of its reservoir host.

ecology↗

Food Supplementation Reduces Nematode Super-Shedding in a Wild Mammal

Anthropogenic changes to the environment, including altered food resource availability, influence host physiology, behaviour, and population dynamics, which can have strong downstream consequences on wildlife disease dynamics. Additionally, some individuals within a population contribute disproportionately to infection as super-shedders of infection, but the extent to which food availability alters the likelihood of super-shedding and overall parasite infection patterns is poorly understood. We conducted a three-year field experiment in southern Finland to investigate how food supplementation and parasite removal affect nematode infection measures and the relationship between nematode infection and fitness of wild bank voles (Clethrionomys glareolus). Using a factorial design across 12 populations, we manipulated food availability and administered anthelmintic treatments to assess effects on nematode infection status, intensity, and two measures of super-shedding (abundance super-shedding, intensity super-shedding). We also examined parasite impacts on host fitness, including apparent survival probability and reproductive status. Food supplementation did not affect likelihood of infection, intensity or intensity super-shedding, but did reduce the likelihood of abundance super-shedding, suggesting an effect of food availability on infection heterogeneity. We also identified an interaction between nematode infection status and host age on fitness. Notably, infected younger individuals had reduced survival and reproduction, but infected older individuals had greater survival and reproduction compared to their uninfected counterparts. Our study provides novel empirical evidence on how anthropogenic changes in food availability can influence parasite transmission dynamics and the fitness consequences of these sub-lethal parasites in a wildlife system.

ecology↗

Ecological factors alter how spatial overlap predicts viral infection dynamics in wild rodent populations

Spatial overlap between animals in wildlife populations can have important implications for pathogen transmission. Ecological factors and animal demographic traits can influence animal space use and spatial overlap, but it is unclear how these interactions drive pathogen transmission. We experimentally manipulated wild bank vole populations via resource supplementation and anthelmintic treatment. Using network analysis, we investigated the relationship between spatial overlap and infection likelihood of an endemic zoonotic hantavirus, including how vole sex and reproductive status interact with spatial behaviour to affect infection likelihood. Spatial overlap in a previous month drove the likelihood of current hantavirus infection, and food supplementation and anthelmintic treatment altered the effects of spatial overlap on infection likelihood. Vole sex and reproductive status were important factors determining whether spatial overlap increased or decreased the likelihood of hantavirus infection and interacted with resource supplementation and anthelmintic treatment, generating different infection dynamics in each treatment. Our research provides rare empirical evidence linking previous spatial overlap to current infection status in wildlife populations, with implications for understanding disease dynamics and persistence as well as developing effective management efforts. We further highlight the importance of incorporating variation in ecological factors and host demography when studying pathogen transmission in wildlife systems.

ecology↗

Effects of Food Addition and Helminth Removal on Space Use and Spatial Overlap in Wild Rodent Populations

1. Animal space use and spatial overlap can have important consequences for population-level processes such as social interactions and pathogen transmission. Identifying how environmental variability and inter-individual variation affect spatial patterns and in turn influence interactions in animal populations is a priority for the study of animal behavior and disease ecology. Environmental food availability and macroparasite infection are common drivers of variation, but there are few experimental studies investigating how they affect spatial patterns of wildlife. 2. Bank voles (Clethrionomys glareolus) are a tractable study system to investigate spatial patterns of wildlife and are amenable to experimental manipulations. We conducted a replicated, factorial field experiment in which we provided supplementary food and removed helminths in vole populations in natural forest habitat and monitored vole space use and spatial overlap using capture-mark-recapture methods. 3. Using network analysis, we quantified vole space use and spatial overlap. We compared the effects of food supplementation and helminth removal and investigated the impact of season, sex, and reproductive status on space use and spatial overlap. 4. We found that food supplementation decreased vole space use while helminth removal increased space use. Space use also varied by sex, reproductive status, and season. Spatial overlap was similar between treatments despite up to three-fold differences in population size. 5. By quantifying the spatial effects of food availability and macroparasite infection on wildlife populations, we demonstrate the potential for space use and population density to trade off and maintain consistent spatial overlap in wildlife populations. This has important implications for spatial processes in wildlife including pathogen transmission.

ecology↗

Paradoxes and synergies: optimizing management of a deadly virus in an endangered carnivore

O_LIPathogen management strategies in wildlife are typically accompanied by an array of uncertainties such as the efficacy of vaccines or potential unintended consequences of interventions. In the context of such uncertainties, models of disease transmission can provide critical insight for optimizing pathogen management, especially for species of conservation concern. The endangered Florida panther experienced an outbreak of feline leukemia virus (FeLV) in 2002-04, and continues to be affected by this deadly virus. Ongoing management efforts aim to mitigate the effects of FeLV on panthers, but with limited information about which strategies may be most effective and efficient. C_LIO_LIWe used a simulation-based approach to determine optimal FeLV management strategies in panthers. We simulated use of proactive FeLV management strategies (i.e., proactive vaccination) and several reactive strategies, including reactive vaccination and test-and-removal. Vaccination strategies accounted for imperfect vaccine-induced immunity, specifically partial immunity in which all vaccinates achieve partial pathogen protection. We compared the effectiveness of these different strategies in mitigating the number of FeLV mortalities and the duration of outbreaks. C_LIO_LIResults showed that inadequate proactive vaccination can paradoxically increase the number of disease-induced mortalities in FeLV outbreaks. These effects were most likely due to imperfect vaccine immunity causing vaccinates to serve as a semi-susceptible population, thereby allowing outbreaks to persist in circumstances otherwise conducive to fadeout. Combinations of proactive vaccination with reactive test-and-removal or vaccination, however, had a synergistic effect in reducing impacts of FeLV outbreaks, highlighting the importance of using mixed strategies in pathogen management. C_LIO_LISynthesis and applications: Management-informed disease simulations are an important tool for identifying unexpected negative consequences and synergies among pathogen management strategies. In particular, we find that imperfect vaccine-induced immunity necessitates further consideration to avoid unintentionally worsening epidemics in some conditions. However, mixing proactive and reactive interventions can improve pathogen control while mitigating uncertainties associated with imperfect interventions. C_LI

ecology↗

Transmission of one predicts another: Apathogenic proxies for transmission dynamics of a fatal virus

Identifying drivers of transmission prior to an epidemic--especially of an emerging pathogen--is a formidable challenge for proactive disease management efforts. We tested a novel approach in the Florida panther, hypothesizing that apathogenic feline immunodeficiency virus (FIV) transmission could predict transmission dynamics for pathogenic feline leukemia virus (FeLV). We derived a transmission network using FIV whole genome sequences, and used exponential random graph models to determine drivers structuring this network. We used these drivers to predict FeLV transmission pathways among panthers and compared predicted outbreak dynamics against empirical FeLV outbreak data. FIV transmission was primarily driven by panther age class and distances between panther home range centroids. Prospective FIV-based modeling predicted FeLV dynamics at least as well as simpler, often retrospective approaches, with evidence that FIV-based predictions captured the spatial structuring of the observed FeLV outbreak. Our finding that an apathogenic agent can predict transmission of an analogously transmitted pathogen is an innovative approach that warrants testing in other host-pathogen systems to determine generalizability. Use of such apathogenic agents holds promise for improving predictions of pathogen transmission in novel host populations, and could thereby provide new strategies for proactive pathogen management in human and animal systems.

ecology↗

Host relatedness and landscape connectivity shape pathogen spread in a large secretive carnivore

Urban expansion can fundamentally alter wildlife movement and gene flow, but how urbanization alters pathogen spread is poorly understood. Here we combine high resolution host and viral genomic data with landscape variables to examine the context of viral spread in puma from two contrasting regions: one bounded by the wildland urban interface (WUI) and one unbounded with minimal anthropogenic development. We found landscape variables and host gene flow explained significant amounts of variation of feline immunodeficiency virus (FIV) spread in the WUI, but not in the unbounded region. The most important predictors of viral spread also differed; host spatial proximity, host relatedness, and mountain ranges played a role in FIV spread in the WUI, whereas unpaved roads were more important in the unbounded region. Our research demonstrates how anthropogenic landscapes can alter pathogen spread, providing a more nuanced understanding of host-pathogen relationships to inform disease ecology in free-ranging species.

ecology↗

A mechanistic, stigmergy model of territory formation in asocial animals: Territorial behavior can dampen disease prevalence but increase persistence

Mechanistic portrayals of how animals form and maintain territories remain rare, and as a discipline, collective movement ecology has tended to focus on synergistic (e.g., migration, shoaling) rather than agonistic or territorial interactions. Here we ask how dynamic territory formation and maintenance might contribute to disease dynamics in an asocial territorial animal for an indirectly transmitted pathogen. We developed a mechanistic individual-based model where stigmergy--the deposition of signals into the environment (e.g., scent marking, scraping)--dictates not only local movement choices and long-term territory formation, but also the risk of pathogen transmission. Based on a variable importance analysis, the length of the infectious period was the single most important variable in predicting outbreak success, maximum prevalence, and outbreak duration. Population size and rate of pathogen decay were also key predictors. We found that territoriality best reduced maximum prevalence in conditions where we would otherwise expect outbreaks to be most successful: slower recovery rates (i.e., longer infectious periods) and higher conspecific densities. However, at high enough densities, outbreak duration became considerably more variable. Our findings therefore support a limited version of the \"territoriality benefits\" hypothesis--where reduced home range overlap leads to reduced opportunities for pathogen transmission, but with the caveat that reduction in outbreak severity may increase the likelihood of pathogen persistence. For longer infectious periods and higher host densities, key trade-offs emerged between the strength of pathogen load, strength of the stigmergy cue, and the rate at which those two quantities decayed; this finding raises interesting questions about the evolutionary nature of these competing processes and the role of possible feedbacks between parasitism and territoriality. This work also highlights the importance of considering social cues as part of the movement landscape in order to improve our understanding of the consequences of individual behaviors on population level outcomes.\n\nAuthor summaryMaking decisions about conservation and disease management relies on our understanding of what allows animal populations to be successful. However, movement ecology, as a field, tends to focus on how animals respond to their abiotic environment. Similarly, disease ecology often focuses on the social behavior of animals without accounting for their individual movement patterns. We developed a simulation model that bridges these two fields by allowing hosts to inform their movement based on the past trajectories of other hosts. As hosts navigate their environment, they leave behind a scent trail while avoiding the scent trails of other individuals. We wanted to know if this means of territory formation could heighten or dampen disease spread when infectious hosts leave pathogens in their wake. We found that territoriality could inhibit disease spread under conditions that we would normally expect pathogens to be most successful: where there are many hosts on the landscape and hosts stay infectious for longer. This work points to how incorporating movement behavior into disease models can provide improved understanding of how diseases spread in wildlife populations; such understanding is particularly important in the face of combatting ongoing and emerging infectious diseases.

ecology↗

Population-Level Disease Dynamics Reflect Individual Heterogeneities in Transmission

Host heterogeneity in disease transmission is widespread and presents a major hurdle to predicting and minimizing pathogen spread. Using the Drosophila melanogaster model system infected with Drosophila C virus, we integrate experimental measurements of individual host heterogeneity in social aggregation, virus shedding, and disease-induced mortality into an epidemiological framework that simulates outbreaks of infectious disease. We use these simulations to calculate individual variation in disease transmission and apportion this variation to specific components of transmission: social network degree distribution, infectiousness, and infection duration. The experimentally-observed variation produces substantial differences in individual transmission potential, providing evidence for genetic and sex-specific effects on disease dynamics at a population level. Manipulating variation in social network connectivity, infectiousness, and infection duration in simulated populations reveals that these components affect disease transmission in clear and distinct ways. We consider the implications of this genetic and sex-specific variation in disease transmission and discuss implications for appropriate control methods given the relative contributions made by social aggregation, virus shedding, and infection duration to transmission in other host-pathogen systems.

ecology↗

Urbanization impacts apex predator gene flow but not genetic diversity across an urban-rural divide

Apex predators are important indicators of intact natural ecosystems. They are also sensitive to urbanization because they require broad home ranges and extensive contiguous habitat to support their prey base. Pumas (Puma concolor) can persist near human developed areas, but urbanization may be detrimental to their movement ecology, population structure, and genetic diversity. To investigate potential effects of urbanization in population connectivity of pumas, we performed a landscape genomics study of 134 pumas on the rural Western Slope and more urbanized Front Range of Colorado, USA. Over 12,000 single nucleotide polymorphisms were genotyped using double-digest, restriction site-associated DNA sequencing (ddRADseq). We investigated patterns of gene flow and genetic diversity, and tested for correlations between key landscape variables and genetic distance to assess the effects of urbanization and other landscape factors on gene flow. Levels of genetic diversity were similar for the Western Slope and Front Range, but effective population sizes were smaller, genetic distances were higher, and there was more overall population substructure in the more urbanized Front Range. Forest cover was strongly positively associated with puma gene flow on the Western Slope, while impervious surfaces restricted gene flow and more open, natural habitats enhanced gene flow on the Front Range. Landscape genomic analyses revealed differences in puma movement and gene flow patterns in rural versus urban settings. Our results highlight the utility of dense, genome-scale markers to document subtle impacts of urbanization on a wide-ranging carnivore living near a large urban center.

genomics↗

How to make more from exposure data? An integrated machine learning pipeline to predict pathogen exposure

O_LIPredicting infectious disease dynamics is a central challenge in disease ecology. Models that can assess which individuals are most at risk of being exposed to a pathogen not only provide valuable insights into disease transmission and dynamics but can also guide management interventions. Constructing such models for wild animal populations, however, is particularly challenging; often only serological data is available on a subset of individuals and non-linear relationships between variables are common.\nC_LIO_LIHere we take advantage of the latest advances in statistical machine learning to construct pathogen-risk models that automatically incorporate complex non-linear relationships with minimal statistical assumptions from ecological data with missing values. Our approach compares multiple machine learning algorithms in a unified environment to find the model with the best predictive performance and uses game theory to better interpret results. We apply this framework on two major pathogens that infect African lions: canine distemper virus (CDV) and feline parvovirus.\nC_LIO_LIOur modelling approach provided enhanced predictive performance compared to more traditional approaches, as well as new insights into disease risks in a wild population. We were able to efficiently capture and visualise strong non-linear patterns, as well as model complex interactions between variables in shaping exposure risk from CDV and feline parvovirus. For example, we found that lions were more likely to be exposed to CDV at a young age but only in low rainfall years.\nC_LIO_LIWhen combined with our data calibration approach, our framework helped us to answer questions about risk of pathogen exposure which are difficult to address with previous methods. Our framework not only has the potential to aid in predicting disease risk in animal populations, but also can be used to build robust predictive models suitable for other ecological applications such as modelling species distribution or diversity patterns.\nC_LI

ecology↗