Patterns and processes of pathogen exposure in gray wolves across North America

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.

Co‐circulation of five species of dog parvoviruses and canine adenovirus type 1 among gray wolves (Canis lupus) in northern Canada

“…Evidence for infection by all investigated dog viruses was found. While CPV‐2 has been found in wild animals all around the planet (Allison et al., 2014; Canuti, Todd et al., 2020; Miranda & Thompson, 2016; Oosthuizen et al., 2019; Steinel et al., 2000; Wang, Tu et al., 2020), and there are reports of CAdV‐1 in wild canids (Balboni et al., 2021; Brandell et al., 2021; Dowgier et al., 2018; Millán et al., 2016; Pizzurro et al., 2017; Walker et al., 2016) and of CBuV‐1 in wolves (Melegari et al., 2019), to the best of our knowledge, this is the first report of MVC, CBoV‐2 and CachaV‐1 in wildlife. Furthermore, our data indicate that CBuV and CachaV‐1 were already circulating among wild animals (i.e., wolves) at least 11 and 10 years before their discoveries, respectively.…”

“…For the last two dog viruses, CAdV‐1 and MVC, low prevalence and low diversity suggest limited spread and/or sporadic introduction. However, seroprevalence data suggest that a high percentage of the wolf population came in contact with the viral species Canine mastadenovirus A (Brandell et al., 2021), which includes CAdV‐1 and CAdV‐2, and the low positivity rate for CAdV‐1 could also be explained by the existence a strong protective immunity due to past infections with one of these two viruses. This could also be true for MVC, but no serological data are available for this virus.…”

“…Like other wild carnivores, the health status of wolf populations can be affected by both enzootic and sporadically introduced pathogens that can cause severe disease, alter reproduction and increase mortality (Balboni et al., 2021; Brand et al., 1995; Brandell et al., 2021). Therefore, acquiring full knowledge of the infectious diseases circulating among wild animals has important implications for population management and control or conservation programs.…”

“…We investigated the presence, diversity and distribution of five different parvoviruses of dogs in a population of wolves inhabiting a vast area of the Northwest Territories, Canada, over a period of 13 years. We also included in the study amdoparvoviruses (genus Amdoparvovirus , subfamily Parvovirinae ) because they are important parvoviruses of carnivores whose host range has only been partially explored (Canuti et al., 2015; Canuti, McDonald et al., 2020), and CAdV‐1 (species Canine adenovirus , genus Mastadenovirus , family Adenoviridae ) because a high seroprevalence of antibodies against this virus was recently identified in wolves in this area (Brandell et al., 2021).…”

Cross‐continental comparison of parasite communities in a wide‐ranging carnivore suggests associations with prey diversity and host density

“…relationship has been demonstrated in nematodes across 19 mammalian species (Arneberg et al, 1998) and relates to increased transmission probabilities as host density increases. Pup mortality and the prevalence of canine distemper virus were both higher in an area of higher wolf density (Almberg et al, 2009), and the relationship between population density and risk of exposure was supported by a broad-scale analysis of pathogens in North American wolves (Brandell et al, 2021). Although gastrointestinal parasites often have minimal effects on host populations, some directly transmitted parasites in this comparative study, including hookworms in the genera Uncinaria and Toxocara and Coccidian protozoans, can cause morbidity or mortality in canids (e.g., Kreeger, 2003;Mech & Kurtz, 1999;Seguel & Gottdenker, 2017), especially in pups or in combination with other stressors (Hudson et al, 2006).…”