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Toxoplasma gondii is a protozoan parasite capable of infecting any warm-blooded species and can increase risk-taking in intermediate hosts. Despite extensive laboratory research on the effects of T. gondii infection on behaviour, little is understood about the effects of toxoplasmosis on wild intermediate host behavior. Yellowstone National Park, Wyoming, USA, has a diverse carnivore community including gray wolves (Canis lupus) and cougars (Puma concolor), intermediate and definitive hosts of T. gondii, respectively. Here, we used 26 years of wolf behavioural, spatial, and serological data to show that wolf territory overlap with areas of high cougar density was an important predictor of infection. In addition, seropositive wolves were more likely to make high-risk decisions such as dispersing and becoming a pack leader, both factors critical to individual fitness and wolf vital rates. Due to the social hierarchy within a wolf pack, we hypothesize that the behavioural effects of toxoplasmosis may create a feedback loop that increases spatial overlap and disease transmission between wolves and cougars. These findings demonstrate that parasites have important implications for intermediate hosts, beyond acute infections, through behavioural impacts. Particularly in a social species, these impacts can surge beyond individuals to affect groups, populations, and even ecosystem processes., (© 2022. The Author(s).)

Helminth infections are cryptic and can be difficult to study in wildlife species. Helminth research in wildlife hosts has historically required invasive animal handling and necropsy, while results from noninvasive parasite research, like scat analysis, may not be possible at the helminth species or individual host levels. To increase the utility of noninvasive sampling, individual hosts can be identified by applying molecular methods. This allows for longitudinal sampling of known hosts and can be paired with individual-level covariates. Here we evaluate a combination of methods and existing long-term monitoring data to identify patterns of cestode infections in gray wolves in Yellowstone National Park. Our goals were: (1) Identify the species and apparent prevalence of cestodes infecting Yellowstone wolves; (2) Assess the relationships between wolf biological and social characteristics and cestode infections; (3) Examine how wolf samples were affected by environmental conditions with respect to the success of individual genotyping. We collected over 200 wolf scats from 2018-2020 and conducted laboratory analyses including individual wolf genotyping, sex identification, cestode identification, and fecal glucocorticoid measurements. Wolf genotyping success rate was 45%, which was higher in the winter but decreased with higher precipitation and as more time elapsed between scat deposit and collection. One cestode species was detected in 28% of all fecal samples, and 38% of known individuals. The most common infection was Echinococcus granulosus sensu lato (primarily E. canadensis). Adult wolves had 4x greater odds of having a cestode infection than pups, as well as wolves sampled in the winter. Our methods provide an alternative approach to estimate cestode prevalence and to linking parasites to known individuals in a wild host system, but may be most useful when employed in existing study systems and when field collections are designed to minimize the time between fecal deposition and collection., Competing Interests: The authors have declared that no competing interests exist., (Copyright: This is an open access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.)

We know much about pathogen evolution and the emergence of new disease strains, but less about host resistance and how it is signaled to other individuals and subsequently maintained. The cline in frequency of black-coated wolves ( Canis lupus ) across North America is hypothesized to result from a relationship with canine distemper virus (CDV) outbreaks. We tested this hypothesis using cross-sectional data from wolf populations across North America that vary in the prevalence of CDV and the allele that makes coats black, longitudinal data from Yellowstone National Park, and modeling. We found that the frequency of CDV outbreaks generates fluctuating selection that results in heterozygote advantage that in turn affects the frequency of the black allele, optimal mating behavior, and black wolf cline across the continent.

Predators may create healthier prey populations by selectively removing diseased individuals. Predators typically prefer some ages of prey over others, which may, or may not, align with those prey ages that are most likely to be diseased. The interaction of age-specific infection and predation has not been previously explored and likely has sizable effects on disease dynamics. We hypothesize that predator cleansing effects will be greater when the disease and predation occur in the same prey age groups. We examine the predator cleansing effect using a model where both vulnerability to predators and pathogen prevalence vary with age. We tailor this model to chronic wasting disease (CWD) in mule deer and elk populations in the Greater Yellowstone Ecosystem, with empirical data from Yellowstone grey wolves and cougars. Model results suggest that under moderate, yet realistic, predation pressure from cougars and wolves independently, predators may decrease CWD outbreak size substantially and delay the accumulation of symptomatic deer and elk. The magnitude of this effect is driven by the ability of predators to selectively remove late-stage CWD infections that are likely the most responsible for transmission, but this may not be the age class they typically select. Thus, predators that select for infected young adults over uninfected juveniles have a stronger cleansing effect, and these effects are strengthened when transmission rates increase with increasing prey morbidity. There are also trade-offs from a management perspective-that is, increasing predator kill rates can result in opposing forces on prey abundance and CWD prevalence. Our modelling exploration shows that predators have the potential to reduce prevalence in prey populations when prey age and disease severity are considered, yet the strength of this effect is influenced by predators' selection for demography or body condition. Current CWD management focuses on increasing cervid hunting as the primary management tool, and our results suggest predators may also be a useful tool under certain conditions, but not necessarily without additional impacts on host abundance and demography. Protected areas with predator populations will play a large role in informing the debate over predator impacts on disease., (© 2022 British Ecological Society.)

The population structure of social species has important consequences for both their demography and transmission of their pathogens. We develop a metapopulation model that tracks two key components of a species' social system: average group size and number of groups within a population. While the model is general, we parameterize it to mimic the dynamics of the Yellowstone wolf population and two associated pathogens: sarcoptic mange and canine distemper. In the initial absence of disease, we show that group size is mainly determined by the birth and death rates and the rates at which groups fission to form new groups. The total number of groups is determined by rates of fission and fusion, as well as environmental resources and rates of intergroup aggression. Incorporating pathogens into the models reduces the size of the host population, predominantly by reducing the number of social groups. Average group size responds in more subtle ways: infected groups decrease in size, but uninfected groups may increase when disease reduces the number of groups and thereby reduces intraspecific aggression. Our modeling approach allows for easy calculation of prevalence at multiple scales (within group, across groups, and population level), illustrating that aggregate population-level prevalence can be misleading for group-living species. The model structure is general, can be applied to other social species, and allows for a dynamic assessment of how pathogens can affect social structure and vice versa., Competing Interests: The authors declare no competing interest.

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.

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., (© 2020 British Ecological Society.)

Population genetic theory posits that molecular variation buffers against disease risk. Although this "monoculture effect" is well supported in agricultural settings, its applicability to wildlife populations remains in question. In the present study, we examined the genomics underlying individual‐level disease severity and population‐level consequences of sarcoptic mange infection in a wild population of canids. Using gray wolves (Canis lupus) reintroduced to Yellowstone National Park (YNP) as our focal system, we leveraged 25 years of observational data and biobanked blood and tissue to genotype 76,859 loci in over 400 wolves. At the individual level, we reported an inverse relationship between host genomic variation and infection severity. We additionally identified 410 loci significantly associated with mange severity, with annotations related to inflammation, immunity, and skin barrier integrity and disorders. We contextualized results within environmental, demographic, and behavioral variables, and confirmed that genetic variation was predictive of infection severity. At the population level, we reported decreased genome‐wide variation since the initial gray wolf reintroduction event and identified evidence of selection acting against alleles associated with mange infection severity. We concluded that genomic variation plays an important role in disease severity in YNP wolves. This role scales from individual to population levels, and includes patterns of genome‐wide variation in support of the monoculture effect and specific loci associated with the complex mange phenotype. Results yielded system‐specific insights, while also highlighting the relevance of genomic analyses to wildlife disease ecology, evolution, and conservation. [ABSTRACT FROM AUTHOR]

Correction to: I Scientific Reports i https://doi.org/10.1038/s41598-021-81192-w, published online 12 February 2021 Heather Fenton was omitted from the author list in the original version of this Article. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health. Financial support includes: E.E.B. and P.J.H. endowment from Verne Willaman; E.E.B. and P.C.C. U.S. Geological Survey (Grant G17AC00427); D.W.S., D.R.S., and D.R.M. NSF LTREB grant DEB-1245373 and many donors to Yellowstone Forever, especially Annie and Bob Graham and Valerie Gates; M.H. Parks Canada and NSF LTREB award 1556248; G.R. Pittman-Robertson Federal Aid in Wildlife Restoration Program and the State of Alaska general funds; K.B. Federal Aid in Support of Wildlife Restoration and Alaska Dept. of Fish and Game; M.A. and H.S. British Columbia Ministry of Forests, Lands, Natural Resource Operations and Rural Development, Habitat Conservation Trust Foundation, Forest Enhancement Society of British Columbia; D.R.M and M.A. Polar Continental Shelf Project and National Geographic Society; M.L.J.G. the Office of the Director, National Institutes of Health under award number NIH T32OD010993; T.W. Ontario Ministry of Natural Resources and Forestry; B.L.B. National Park Service; A.K. GNWT Environmental Stewardship Fund. [Extracted from the article]