Sarcoptic mange severity is associated with reduced genomic variation and evidence of selection in Yellowstone National Park wolves (Canis lupus).
ABSTRACT: 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.
Project description:The "itch mite" or "mange mite", <i>Sarcoptes scabiei,</i> causes scabies in humans and sarcoptic mange in domestic and free-ranging animals. This mite has a wide host range due to its ability to adapt to new hosts and has been spread across the globe presumably through human expansion. While disease caused by <i>S. scabiei</i> has been very well-studied in humans and domestic animals, there are still numerous gaps in our understanding of this pathogen in free-ranging wildlife. The literature on sarcoptic mange in North American wildlife is particularly limited, which may be due to the relatively limited number of clinically-affected species and lack of severe population impacts seen in other continents. This review article provides a summary of the current knowledge of mange in wildlife, with a focus on the most common clinically-affected species in North America including red foxes (<i>Vulpes vulpes</i>), gray wolves (<i>Canis lupus</i>), coyotes (<i>Canis latrans</i>), and American black bears (<i>Ursus americanus</i>).
Project description:Sarcoptic mange, a parasitic disease caused by the mite Sarcoptes scabiei, is regularly reported on wolves Canis lupus in Scandinavia. We describe the distribution and transmission of this parasite within the small but recovering wolf population by analysing 269 necropsy reports and performing a serological survey on 198 serum samples collected from free-ranging wolves between 1998 and 2013.The serological survey among 145 individual captured Scandinavian wolves (53 recaptures) shows a consistent presence of antibodies against sarcoptic mange. Seropositivity among all captured wolves was 10.1 % (CI. 6.4 %-15.1 %). Sarcoptic mange-related mortality reported at necropsy was 5.6 % and due to secondary causes, predominantly starvation. In the southern range of the population, seroprevalence was higher, consistent with higher red fox densities. Female wolves had a lower probability of being seropositive than males, but for both sexes the probability increased with pack size. Recaptured individuals changing from seropositive to seronegative suggest recovery from sarcoptic mange. The lack of seropositive pups (8-10 months, N?=?56) and the occurrence of seropositive and seronegative individuals in the same pack indicates interspecific transmission of S. scabiei into this wolf population.We consider sarcoptic mange to have little effect on the recovery of the Scandinavian wolf population. Heterogenic infection patterns on the pack level in combination with the importance of individual-based factors (sex, pack size) and the north-south gradient for seroprevalence suggests low probability of wolf-to-wolf transmission of S. scabiei in Scandinavia.
Project description:Sarcoptic mange is globally enzootic, and non-invasive methods with high diagnostic specificity for its surveillance in wildlife are lacking. We describe the molecular detection of <i>Sarcoptes scabiei</i> in non-invasively collected faecal samples, targeting the 16S rDNA gene. We applied this method to 843 Iberian wolf <i>Canis lupus signatus</i> faecal samples collected in north-western Portugal (2006-2018). We further integrated this with serological data (61 samples from wolf and 20 from red fox <i>Vulpes vulpes</i>, 1997-2019) in multi-event capture-recapture models. The mean predicted prevalence by the molecular analysis of wolf faecal samples from 2006-2018 was 7.2% (CI<sub>95</sub> 5.0-9.4%; range: 2.6-11.7%), highest in 2009. The mean predicted seroprevalence in wolves was 24.5% (CI<sub>95</sub> 18.5-30.6%; range: 13.0-55.0%), peaking in 2006-2009. Multi-event capture-recapture models estimated 100% diagnostic specificity and moderate diagnostic sensitivity (30.0%, CI<sub>95</sub> 14.0-53.0%) for the molecular method. Mange-infected individually identified wolves showed a tendency for higher mortality versus uninfected wolves (?Mortality 0.150, CI<sub>95</sub> -0.165-0.458). Long-term serology data highlights the endemicity of sarcoptic mange in wild canids but uncovers multi-year epidemics. This study developed and evaluated a novel method for surveying sarcoptic mange in wildlife populations by the molecular detection of <i>S. scabiei</i> in faecal samples, which stands out for its high specificity and non-invasive character.
Project description:The desire to see free ranging large carnivores in their natural habitat is a driver of tourism in protected areas around the globe. However, large carnivores are wide-ranging and subject to human-caused mortality outside protected area boundaries. The impact of harvest (trapping or hunting) on wildlife viewing opportunities has been the subject of intense debate and speculation, but quantitative analyses have been lacking. We examined the effect of legal harvest of wolves (Canis lupus) along the boundaries of two North American National Parks, Denali (DNPP) and Yellowstone (YNP), on wolf viewing opportunities within the parks during peak tourist season. We used data on wolf sightings, pack sizes, den site locations, and harvest adjacent to DNPP from 1997-2013 and YNP from 2008-2013 to evaluate the relationship between harvest and wolf viewing opportunities. Although sightings were largely driven by wolf population size and proximity of den sites to roads, sightings in both parks were significantly reduced by harvest. Sightings in YNP increased by 45% following years with no harvest of a wolf from a pack, and sightings in DNPP were more than twice as likely during a period with a harvest buffer zone than in years without the buffer. These findings show that harvest of wolves adjacent to protected areas can reduce sightings within those areas despite minimal impacts on the size of protected wolf populations. Consumptive use of carnivores adjacent to protected areas may therefore reduce their potential for non-consumptive use, and these tradeoffs should be considered when developing regional wildlife management policies.
Project description:BACKGROUND:Gray wolves (Canis lupus) were reintroduced into Yellowstone National Park (YNP) after a >70 year absence, and as part of recovery efforts, the population has been closely monitored. In 1999 and 2005, pup survival was significantly reduced, suggestive of disease outbreaks. METHODOLOGY/PRINCIPAL FINDINGS:We analyzed sympatric wolf, coyote (Canis latrans), and red fox (Vulpes vulpes) serologic data from YNP, spanning 1991-2007, to identify long-term patterns of pathogen exposure, identify associated risk factors, and examine evidence for disease-induced mortality among wolves for which there were survival data. We found high, constant exposure to canine parvovirus (wolf seroprevalence: 100%; coyote: 94%), canine adenovirus-1 (wolf pups [0.5-0.9 yr]: 91%, adults [>or=1 yr]: 96%; coyote juveniles [0.5-1.5 yrs]: 18%, adults [>or=1.6 yrs]: 83%), and canine herpesvirus (wolf: 87%; coyote juveniles: 23%, young adults [1.6-4.9 yrs]: 51%, old adults [>or=5 yrs]: 87%) suggesting that these pathogens were enzootic within YNP wolves and coyotes. An average of 50% of wolves exhibited exposure to the protozoan parasite, Neospora caninum, although individuals' odds of exposure tended to increase with age and was temporally variable. Wolf, coyote, and fox exposure to canine distemper virus (CDV) was temporally variable, with evidence for distinct multi-host outbreaks in 1999 and 2005, and perhaps a smaller, isolated outbreak among wolves in the interior of YNP in 2002. The years of high wolf-pup mortality in 1999 and 2005 in the northern region of the park were correlated with peaks in CDV seroprevalence, suggesting that CDV contributed to the observed mortality. CONCLUSIONS/SIGNIFICANCE:Of the pathogens we examined, none appear to jeopardize the long-term population of canids in YNP. However, CDV appears capable of causing short-term population declines. Additional information on how and where CDV is maintained and the frequency with which future epizootics might be expected might be useful for future management of the Northern Rocky Mountain wolf population.
Project description:BACKGROUND:Sarcoptic mange, caused by the Sarcoptes scabiei mite, is an infectious disease of wildlife, domestic animals and humans with international importance. Whilst a variety of treatment and control methods have been investigated in wildlife, the literature is fragmented and lacking consensus. The primary objectives of this review were to synthesise the diverse literature published on the treatment of sarcoptic mange in wildlife from around the world, and to identify the qualities of successful treatment strategies in both captive and free-roaming wildlife. METHODS:A systematic search of the electronic databases CAB Direct, PubMed, Scopus, Web of Science, EMBASE and Discovery was undertaken. Data pertaining to study design, country, year, species, study size, mange severity, treatment protocol and outcomes were extracted from eligible studies and placed in a table. Following data extraction, a decision tree was used to identify studies suitable for further analysis based on the effectiveness of their treatment protocol, whether they were conducted on captive or non-captive wildlife, and the quality of their post-treatment monitoring period. RESULTS:Twenty-eight studies met our initial inclusion criteria for data collection. Of these studies, 15 were selected for further analysis following application of the decision tree. This comprised of 9 studies on captive wildlife, 5 studies on free-living wildlife and 1 study involving both captive and free-living wildlife. Ivermectin delivered multiple times via subcutaneous injection at a dose between 200-400 µg/kg was found to be the most common and successfully used treatment, although long-term data on post-release survival and re-infection rates was elusive. CONCLUSIONS:To our knowledge, this review is the first to demonstrate that multiple therapeutic protocols exist for the treatment of sarcoptic mange in wildlife. However, several contemporary treatment options are yet to be formally reported in wildlife, such as the use of isoxazoline chemicals as a one-off treatment. There is also a strong indication for more randomised controlled trials, as well as improved methods of post-treatment monitoring. Advancing this field of knowledge is expected to aid veterinarians, wildlife workers and policy makers with the design and implementation of effective treatment and management strategies for the conservation of wildlife affected by sarcoptic mange.
Project description:<h4>Background</h4>Pastoralists in low-income countries usually live in close proximity to their animals and thus represent an important repository of information about livestock disease. Since wild and domestic animals often mix freely whilst grazing, pastoralists are also able to observe first-hand the diseases that are present in wildlife and as such are key informants in disease outbreaks in sylvatic animals. We report here the findings of the first study of the knowledge and role of Masai pastoralists in mange in wildlife and livestock in Masai Mara, Kenya.<h4>Methodology/principal findings</h4>In this paper we describe the knowledge of mange accrued by 56 Masai pastoralists in Kenya and how they respond to it in both wildlife and livestock. In total, 52 (93%) pastoralists had a clear idea of the clinical appearance of mange, 13 (23%) understood its aetiology and 37 (66%) knew that mites were the causal agent. Thirty-nine (69%) believed that mange cross-infection between domestic and wild animals occurs, while 48 (85%) had observed mange in domestic animals including sheep (77%), goats (57%), dogs (24%) and cattle (14%). The pastoralists had also observed wild animals infected with mange, above all lions (19%), gazelles (14%), cheetahs (12%) and wildebeests (2%). In 68% of cases Masai pastoralists treat mange infection or apply control measures, most commonly via the topical use of acaricides (29%) and/or the reporting of the outbreak to the veterinary authorities (21%). In the period 2007-2011, Kenya Wildlife Service received 24 warnings of 59 wild animals with mange-like lesions from the Masai Mara pastoralist community. The reported species were cheetah, lion, wild dog, Thomson's gazelle and wildebeest.<h4>Conclusion</h4>Masai pastoralists have good knowledge of mange epidemiology and treatment. Their observations and the treatments they apply are valuable in the control of this disease in both wild and domestic animals.
Project description:Sarcoptic mange, caused by the parasitic mite Sarcoptes scabiei, causes a substantive burden of disease to humans, domestic animals and wildlife, globally. There are many effects of S. scabiei infection, culminating in the disease which hosts suffer. However, major knowledge gaps remain on the pathogenic impacts of this infection. Here, we focus on the bare-nosed wombat host (Vombatus ursinus) to investigate the effects of mange on: (i) host heat loss and thermoregulation, (ii) field metabolic rates, (iii) foraging and resting behaviour across full circadian cycles, and (iv) fatty acid composition in host adipose, bone marrow, brain and muscle tissues. Our findings indicate that mange-infected V. ursinus lose more heat to the environment from alopecia-affected body regions than healthy individuals. Additionally, mange-infected individuals have higher metabolic rates in the wild. However, these metabolic demands are difficult to meet, because infected individuals spend less time foraging and more time inactive relative to their healthy counterparts, despite being outside of the burrow for longer. Lastly, mange infection results in altered fatty acid composition in adipose tissue, with increased amounts of omega-6 acids, and decreased amounts of omega-3 acids, a consequence of chronic cutaneous inflammation and inhibition of anti-inflammatory responses. These findings highlight the interactions of mange-induced physiological and behavioural changes, and have implications for the treatment and rehabilitation of infected individuals.
Project description:This letter comments on the article "The treatment of sarcoptic mange in wildlife: a systematic review" published in Parasites & Vectors 2019, 12:99, and discusses the limitations in the use of endectocides for scabies control in free-ranging wildlife. The ecological impact and drug resistance to ivermectin are also discussed. In our view, scabies control in free-ranging wildlife should be based preferably on population management measures, and whether to apply individual treatments to free-ranging populations should be considered very carefully and avoided where not absolutely warranted.
Project description:<h4>Background</h4>Many western European carnivore populations became almost or completely eradicated during the last ~200 years, but are now recovering. Extirpation of wolves started in Finland in the 19th century, and for more than 150 years the population size of wolves has remained small. To investigate historical patterns of genetic variation, we extracted DNA from 114 wolf samples collected in zoological museums over the last ~150 years. Fifteen microsatellite loci were used to look at genotypic variation in this historical sample. Additionally, we amplified a 430 bp sequence of mtDNA control region from the same samples. Contemporary wolf samples (N?=?298) obtained after the population recovery in the mid-1990s, were used as a reference.<h4>Results</h4>Our analyses of mtDNA revealed reduced variation in the mtDNA control region through the loss of historical haplotypes observed prior to wolf declines. Heterozygosity at autosomal microsatellite loci did not decrease significantly. However, almost 20% of microsatellite alleles were unique to wolves collected before the 1960s. The genetic composition of the population changed gradually with the largest changes occurring prior to 1920. Half of the oldest historical samples formed a distinguishable genetic cluster not detected in the modern-day Finnish or Russian samples, and might therefore represent northern genetic variation lost from today's gene pool. Point estimates of Ne were small (13.2 and 20.5) suggesting population fragmentation. Evidence of a genetic population bottleneck was also detected.<h4>Conclusions</h4>Our genetic analyses confirm changes in the genetic composition of the Finnish wolf population through time, despite the geographic interconnectivity to a much larger population in Russia. Our results emphasize the need for restoration of the historical connectivity between the present wolf populations to secure long-term viability. This might be challenging, however, because the management policies between Western and Eastern Europe often differ greatly. Additionally, wolf conservation is still a rather controversial issue, and anthropogenic pressure towards wolves remains strong.