ABSTRACT
Chronic wasting disease (CWD) is a fatal prion disease of cervids that has spread across much of North America. Although gold standard CWD diagnostics involve postmortem testing of medial retropharyngeal lymph nodes or obex (brain stem), a key tissue sample for antemortem testing is rectoanal mucosa-associated lymphoid tissue (RAMALT). However, collection of an adequate sample (i.e., enough lymphoid follicles) may be affected by factors such as deer age, repeated sampling, skill of the sampler, and adverse conditions during collection. Here, we document the protocol used to train personnel for RAMALT collection in a large study of free-ranging white-tailed deer (Odocoileus virginianus) in Wisconsin, USA, and determine factors that contributed to the occurrence of inadequate RAMALT samples. Our training protocol included hands-on experience with postmortem tissues, as well as a mentored collection process in the field. Collection of RAMALT under field conditions was highly successful, with 763/806 (94.7%) samples deemed adequate for subsequent testing. Although inadequate samples were rare, they were more likely to occur with older deer and when samples were collected at dusk (i.e., limited ambient lighting). We conclude that RAMALT collection can be highly successful under adverse field conditions, including with technicians with limited prior veterinary experience, and we provide details of our training program to facilitate repeatability in other antemortem CWD testing efforts.
ABSTRACT
With emerging infectious disease outbreaks in human, domestic and wild animal populations on the rise, improvements in pathogen characterization and surveillance are paramount for the protection of human and animal health, as well as the conservation of ecologically and economically important wildlife. Genomics offers a range of suitable tools to meet these goals, with metagenomic sequencing facilitating the characterization of whole microbial communities associated with emerging and endemic disease outbreaks. Here, we use metagenomic sequencing in a case-control study to identify microbes in lung tissue associated with newly observed pneumonia-related fatalities in 34 white-tailed deer (Odocoileus virginianus) in Wisconsin, USA. We identified 20 bacterial species that occurred in more than a single individual. Of these, only Clostridium novyi was found to substantially differ (in number of detections) between case and control sample groups; however, this difference was not statistically significant. We also detected several bacterial species associated with pneumonia and/or other diseases in ruminants (Mycoplasma ovipneumoniae, Trueperella pyogenes, Pasteurella multocida, Anaplasma phagocytophilum, Fusobacterium necrophorum); however, these species did not substantially differ between case and control sample groups. On average, we detected a larger number of bacterial species in case samples than controls, supporting the potential role of polymicrobial infections in this system. Importantly, we did not detect DNA of viruses or fungi, suggesting that they are not significantly associated with pneumonia in this system. Together, these results highlight the utility of metagenomic sequencing for identifying disease-associated microbes. This preliminary list of microbes will help inform future research on pneumonia-associated fatalities of white-tailed deer.
Subject(s)
Deer , Pneumonia , Animals , Humans , Case-Control Studies , Metagenomics , Animals, WildABSTRACT
Seasonal variation in habitat use and animal behavior can alter host contact patterns with potential consequences for pathogen transmission dynamics. The endangered Florida panther (Puma concolor coryi) has experienced significant pathogen-induced mortality and continues to be at risk of future epidemics. Prior research has found increased panther movement in Florida's dry versus wet seasons, which may affect panther population connectivity and seasonally increase potential pathogen transmission. Our objective was to determine if Florida panthers are more spatially connected in dry seasons relative to wet seasons, and test if identified connectivity differences resulted in divergent predicted epidemic dynamics. We leveraged extensive panther telemetry data to construct seasonal panther home range overlap networks over an 11 year period. We tested for differences in network connectivity, and used observed network characteristics to simulate transmission of a broad range of pathogens through dry and wet season networks. We found that panthers were more spatially connected in dry seasons than wet seasons. Further, these differences resulted in a trend toward larger and longer pathogen outbreaks when epidemics were initiated in the dry season. Our results demonstrate that seasonal variation in behavioral patterns-even among largely solitary species-can have substantial impacts on epidemic dynamics.
Subject(s)
Disease Outbreaks , Animals , SeasonsABSTRACT
Close contacts between individuals provide opportunities for the transmission of diseases, including COVID-19. While individuals take part in many different types of interactions, including those with classmates, co-workers and household members, it is the conglomeration of all of these interactions that produces the complex social contact network interconnecting individuals across the population. Thus, while an individual might decide their own risk tolerance in response to a threat of infection, the consequences of such decisions are rarely so confined, propagating far beyond any one person. We assess the effect of different population-level risk-tolerance regimes, population structure in the form of age and household-size distributions, and different interaction types on epidemic spread in plausible human contact networks to gain insight into how contact network structure affects pathogen spread through a population. In particular, we find that behavioural changes by vulnerable individuals in isolation are insufficient to reduce those individuals' infection risk and that population structure can have varied and counteracting effects on epidemic outcomes. The relative impact of each interaction type was contingent on assumptions underlying contact network construction, stressing the importance of empirical validation. Taken together, these results promote a nuanced understanding of disease spread on contact networks, with implications for public health strategies.
ABSTRACT
Pathogen 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.We 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.Results 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.Synthesis 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.
ABSTRACT
BACKGROUND: Dispersal is a fundamental process to animal population dynamics and gene flow. In white-tailed deer (WTD; Odocoileus virginianus), dispersal also presents an increasingly relevant risk for the spread of infectious diseases. Across their wide range, WTD dispersal is believed to be driven by a suite of landscape and host behavioral factors, but these can vary by region, season, and sex. Our objectives were to (1) identify dispersal events in Wisconsin WTD and determine drivers of dispersal rates and distances, and (2) determine how landscape features (e.g., rivers, roads) structure deer dispersal paths. METHODS: We developed an algorithmic approach to detect dispersal events from GPS collar data for 590 juvenile, yearling, and adult WTD. We used statistical models to identify host and landscape drivers of dispersal rates and distances, including the role of agricultural land use, the traversability of the landscape, and potential interactions between deer. We then performed a step selection analysis to determine how landscape features such as agricultural land use, elevation, rivers, and roads affected deer dispersal paths. RESULTS: Dispersal predominantly occurred in juvenile males, of which 64.2% dispersed, with dispersal events uncommon in other sex and age classes. Juvenile male dispersal probability was positively associated with the proportion of the natal range that was classified as agricultural land use, but only during the spring. Dispersal distances were typically short (median 5.77 km, range: 1.3-68.3 km), especially in the fall. Further, dispersal distances were positively associated with agricultural land use in potential dispersal paths but negatively associated with the number of proximate deer in the natal range. Lastly, we found that, during dispersal, juvenile males typically avoided agricultural land use but selected for areas near rivers and streams. CONCLUSION: Land use-particularly agricultural-was a key driver of dispersal rates, distances, and paths in Wisconsin WTD. In addition, our results support the importance of deer social environments in shaping dispersal behavior. Our findings reinforce knowledge of dispersal ecology in WTD and how landscape factors-including major rivers, roads, and land-use patterns-structure host gene flow and potential pathogen transmission.
ABSTRACT
White-tailed deer (WTD; Odocoileus virginianus) are a critical species for ecosystem function and wildlife management. As such, studies of cause-specific mortality among WTD have long been used to understand population dynamics. However, detailed pathological information is rarely documented for free-ranging WTD, especially in regions with a high prevalence of chronic wasting disease (CWD). This leaves a significant gap in understanding how CWD is associated with disease processes or comorbidities that may subsequently alter broader population dynamics. We investigated unknown mortalities among collared WTD in southwestern Wisconsin, USA, an area of high CWD prevalence. We tested for associations between CWD and other disease processes and used a network approach to test for co-occurring disease processes. Predation and infectious disease were leading suspected causes of death, with high prevalence of CWD (42.4%; of 245 evaluated) and pneumonia (51.2%; of 168 evaluated) in our sample. CWD prevalence increased with age, before decreasing among older individuals, with more older females than males in our sample. Females were more likely to be CWD positive, and although this was not statistically significant when accounting for age, females were significantly more likely to die with end-stage CWD than males and may consequently be an underrecognized source of CWD transmission. Presence of CWD was associated with emaciation, atrophy of marrow fat and hematopoietic cells, and ectoparasitism (lice and ticks). Occurrences of severe infectious disease processes clustered together (e.g., pneumonia, CWD), as compared to noninfectious or low-severity processes (e.g., sarcocystosis), although pneumonia cases were not fully explained by CWD status. With the prevalence of CWD increasing across North America, our results highlight the critical importance of understanding the potential role of CWD in favoring or maintaining disease processes of importance for deer population health and dynamics.
Subject(s)
Communicable Diseases , Deer , Wasting Disease, Chronic , Animals , Cause of Death , Communicable Diseases/veterinary , Ecosystem , Wasting Disease, Chronic/epidemiology , WisconsinABSTRACT
Identifying drivers of transmission-especially of emerging pathogens-is a formidable challenge for proactive disease management efforts. While close social interactions can be associated with microbial sharing between individuals, and thereby imply dynamics important for transmission, such associations can be obscured by the influences of factors such as shared diets or environments. Directly-transmitted viral agents, specifically those that are rapidly evolving such as many RNA viruses, can allow for high-resolution inference of transmission, and therefore hold promise for elucidating not only which individuals transmit to each other, but also drivers of those transmission events. Here, we tested a novel approach in the Florida panther, which is affected by several directly-transmitted feline retroviruses. We first inferred the transmission network for an apathogenic, directly-transmitted retrovirus, feline immunodeficiency virus (FIV), and then used exponential random graph models to determine drivers structuring this network. We then evaluated the utility of these drivers in predicting transmission of the analogously transmitted, pathogenic agent, feline leukemia virus (FeLV), and compared FIV-based predictions of outbreak dynamics against empirical FeLV outbreak data. FIV transmission was primarily driven by panther age class and distances between panther home range centroids. FIV-based modeling predicted FeLV dynamics similarly to common modeling approaches, but with evidence that FIV-based predictions captured the spatial structuring of the observed FeLV outbreak. While FIV-based predictions of FeLV transmission performed only marginally better than standard approaches, our results highlight the value of proactively identifying drivers of transmission-even based on analogously-transmitted, apathogenic agents-in order to predict transmission of emerging infectious agents. The identification of underlying drivers of transmission, such as through our workflow here, therefore holds promise for improving predictions of pathogen transmission in novel host populations, and could provide new strategies for proactive pathogen management in human and animal systems.
ABSTRACT
Pathogen transmission depends on host density, mobility and contact. These components emerge from host and pathogen movements that themselves arise through interactions with the surrounding environment. The environment, the emergent host and pathogen movements, and the subsequent patterns of density, mobility and contact form an 'epidemiological landscape' connecting the environment to specific locations where transmissions occur. Conventionally, the epidemiological landscape has been described in terms of the geographical coordinates where hosts or pathogens are located. We advocate for an alternative approach that relates those locations to attributes of the local environment. Environmental descriptions can strengthen epidemiological forecasts by allowing for predictions even when local geographical data are not available. Environmental predictions are more accessible than ever thanks to new tools from movement ecology, and we introduce a 'movement-pathogen pace of life' heuristic to help identify aspects of movement that have the most influence on spatial epidemiology. By linking pathogen transmission directly to the environment, the epidemiological landscape offers an efficient path for using environmental information to inform models describing when and where transmission will occur.
Subject(s)
Disease Transmission, Infectious , Ecology , Epidemiology , Movement , GeographyABSTRACT
Hunting can fundamentally alter wildlife population dynamics but the consequences of hunting on pathogen transmission and evolution remain poorly understood. Here, we present a study that leverages a unique landscape-scale quasi-experiment coupled with pathogen-transmission tracing, network simulation and phylodynamics to provide insights into how hunting shapes feline immunodeficiency virus (FIV) dynamics in puma (Puma concolor). We show that removing hunting pressure enhances the role of males in transmission, increases the viral population growth rate and increases the role of evolutionary forces on the pathogen compared to when hunting was reinstated. Changes in transmission observed with the removal of hunting could be linked to short-term social changes while the male puma population increased. These findings are supported through comparison with a region with stable hunting management over the same time period. This study shows that routine wildlife management can have impacts on pathogen transmission and evolution not previously considered.
Subject(s)
Immunodeficiency Virus, Feline , Puma , Animals , Animals, Wild , Female , Immunodeficiency Virus, Feline/physiology , Male , Predatory Behavior , Puma/physiology , Puma/virology , Virus Physiological PhenomenaABSTRACT
Network analysis of infectious disease in wildlife can reveal traits or individuals critical to pathogen transmission and help inform disease management strategies. However, estimates of contact between animals are notoriously difficult to acquire. Researchers commonly use telemetry technologies to identify animal associations; but such data may have different sampling intervals and often captures a small subset of the population. The objectives of this study were to outline best practices for telemetry sampling in network studies of infectious disease by determining (1) the consequences of telemetry sampling on our ability to estimate network structure, (2) whether contact networks can be approximated using purely spatial contact definitions, and (3) how wildlife spatial configurations may influence telemetry sampling requirements.We simulated individual movement trajectories for wildlife populations using a home range-like movement model, creating full location datasets and corresponding "complete" networks. To mimic telemetry data, we created "sample" networks by subsampling the population (10-100% of individuals) with a range of sampling intervals (every minute to every three days). We varied the definition of contact for sample networks, using either spatiotemporal or spatial overlap, and varied the spatial configuration of populations (random, lattice, or clustered). To compare complete and sample networks, we calculated seven network metrics important for disease transmission and assessed mean ranked correlation coefficients and percent error between complete and sample network metrics.Telemetry sampling severely reduced our ability to calculate global node-level network metrics, but had less impact on local and network-level metrics. Even so, in populations with infrequent associations, high intensity telemetry sampling may still be necessary. Defining contact in terms of spatial overlap generally resulted in overly connected networks, but in some instances, could compensate for otherwise coarse telemetry data.By synthesizing movement and disease ecology with computational approaches, we characterized trade-offs important for using wildlife telemetry data beyond ecological studies of individual movement, and found that careful use of telemetry data has the potential to inform network models. Thus, with informed application of telemetry data, we can make significant advances in leveraging its use for a better understanding and management of wildlife infectious disease.
ABSTRACT
The presence of many pathogens varies in a predictable manner with latitude, with infections decreasing from the equator towards the poles. We investigated the geographic trends of pathogens infecting a widely distributed carnivore: the gray wolf (Canis lupus). Specifically, we investigated which variables best explain and predict geographic trends in seroprevalence across North American wolf populations and the implications of the underlying mechanisms. We compiled a large serological dataset of nearly 2000 wolves from 17 study areas, spanning 80° longitude and 50° latitude. Generalized linear mixed models were constructed to predict the probability of seropositivity of four important pathogens: canine adenovirus, herpesvirus, parvovirus, and distemper virus-and two parasites: Neospora caninum and Toxoplasma gondii. Canine adenovirus and herpesvirus were the most widely distributed pathogens, whereas N. caninum was relatively uncommon. Canine parvovirus and distemper had high annual variation, with western populations experiencing more frequent outbreaks than eastern populations. Seroprevalence of all infections increased as wolves aged, and denser wolf populations had a greater risk of exposure. Probability of exposure was positively correlated with human density, suggesting that dogs and synanthropic animals may be important pathogen reservoirs. Pathogen exposure did not appear to follow a latitudinal gradient, with the exception of N. caninum. Instead, clustered study areas were more similar: wolves from the Great Lakes region had lower odds of exposure to the viruses, but higher odds of exposure to N. caninum and T. gondii; the opposite was true for wolves from the central Rocky Mountains. Overall, mechanistic predictors were more informative of seroprevalence trends than latitude and longitude. Individual host characteristics as well as inherent features of ecosystems determined pathogen exposure risk on a large scale. This work emphasizes the importance of biogeographic wildlife surveillance, and we expound upon avenues of future research of cross-species transmission, spillover, and spatial variation in pathogen infection.
Subject(s)
Environmental Exposure , Epidemiological Models , Infections/veterinary , Wolves/virology , Animals , Anthropogenic Effects , Female , Humans , Infections/epidemiology , Infections/etiology , Infections/transmission , Male , North America/epidemiology , Seroepidemiologic Studies , Wolves/parasitologyABSTRACT
The spatial organization of a population can influence the spread of information, behaviour and pathogens. Group territory size and territory overlap and components of spatial organization, provide key information as these metrics may be indicators of habitat quality, resource dispersion, contact rates and environmental risk (e.g. indirectly transmitted pathogens). Furthermore, sociality and behaviour can also shape space use, and subsequently, how space use and habitat quality together impact demography. Our study aims to identify factors shaping the spatial organization of wildlife populations and assess the impact of epizootics on space use. We further aim to explore the mechanisms by which disease perturbations could cause changes in spatial organization. Here we assessed the seasonal spatial organization of Serengeti lions and Yellowstone wolves at the group level. We use network analysis to describe spatial organization and connectivity of social groups. We then examine the factors predicting mean territory size and mean territory overlap for each population using generalized additive models. We demonstrate that lions and wolves were similar in that group-level factors, such as number of groups and shaped spatial organization more than population-level factors, such as population density. Factors shaping territory size were slightly different than factors shaping territory overlap; for example, wolf pack size was an important predictor of territory overlap, but not territory size. Lion spatial networks were more highly connected, while wolf spatial networks varied seasonally. We found that resource dispersion may be more important for driving territory size and overlap for wolves than for lions. Additionally, canine distemper epizootics may have altered lion spatial organization, highlighting the importance of including infectious disease epizootics in studies of behavioural and movement ecology. We provide insight about when we might expect to observe the impacts of resource dispersion, disease perturbations, and other ecological factors on spatial organization. Our work highlights the importance of monitoring and managing social carnivore populations at the group level. Future research should elucidate the complex relationships between demographics, social and spatial structure, abiotic and biotic conditions and pathogen infections.
Subject(s)
Carnivora , Lions , Wolves , Animals , Ecosystem , SeasonsABSTRACT
The outbreak and transmission of disease-causing pathogens are contributing to the unprecedented rate of biodiversity decline. Recent advances in genomics have coalesced into powerful tools to monitor, detect, and reconstruct the role of pathogens impacting wildlife populations. Wildlife researchers are thus uniquely positioned to merge ecological and evolutionary studies with genomic technologies to exploit unprecedented "Big Data" tools in disease research; however, many researchers lack the training and expertise required to use these computationally intensive methodologies. To address this disparity, the inaugural "Genomics of Disease in Wildlife" workshop assembled early to mid-career professionals with expertise across scientific disciplines (e.g., genomics, wildlife biology, veterinary sciences, and conservation management) for training in the application of genomic tools to wildlife disease research. A horizon scanning-like exercise, an activity to identify forthcoming trends and challenges, performed by the workshop participants identified and discussed 5 themes considered to be the most pressing to the application of genomics in wildlife disease research: 1) "Improving communication," 2) "Methodological and analytical advancements," 3) "Translation into practice," 4) "Integrating landscape ecology and genomics," and 5) "Emerging new questions." Wide-ranging solutions from the horizon scan were international in scope, itemized both deficiencies and strengths in wildlife genomic initiatives, promoted the use of genomic technologies to unite wildlife and human disease research, and advocated best practices for optimal use of genomic tools in wildlife disease projects. The results offer a glimpse of the potential revolution in human and wildlife disease research possible through multi-disciplinary collaborations at local, regional, and global scales.
Subject(s)
Animal Diseases/etiology , Animals, Wild , Genomics , Research , Animal Diseases/epidemiology , Animal Diseases/transmission , Animals , Biodiversity , Biological Evolution , Computational Biology/methods , Disease Susceptibility , Ecology , Environment , Genome , Genomics/methods , Host-Pathogen Interactions/genetics , HumansABSTRACT
Utilization of contact networks has provided opportunities for assessing the dynamic interplay between pathogen transmission and host behavior. Genomic techniques have, in their own right, provided new insight into complex questions in disease ecology, and the increasing accessibility of genomic approaches means more researchers may seek out these tools. The integration of network and genomic approaches provides opportunities to examine the interaction between behavior and pathogen transmission in new ways and with greater resolution. While a number of studies have begun to incorporate both contact network and genomic approaches, a great deal of work has yet to be done to better integrate these techniques. In this review, we give a broad overview of how network and genomic approaches have each been used to address questions regarding the interaction of social behavior and infectious disease, and then discuss current work and future horizons for the merging of these techniques.