Sarcoptic mange is a highly contagious skin disease caused by the ectoparasitic mite Sarcoptes scabiei. Although it afflicts over 100 mammal species worldwide, sarcoptic mange remains a disease ...obscured by variability at the individual, population and species levels. Amid this variability, it is critical to identify consistent drivers of morbidity, particularly at the skin barrier.
Using culture-independent next generation sequencing, we characterized the skin microbiome of three species of North American canids: coyotes (Canis latrans), red foxes (Vulpes vulpes) and gray foxes (Urocyon cinereoargenteus). We compared alpha and beta diversity between mange-infected and uninfected canids using the Kruskal-Wallis test and multivariate analysis of variance with permutation. We used analysis of composition of microbes and gneiss balances to perform differential abundance testing between infection groups.
We found remarkably consistent signatures of microbial dysbiosis associated with mange infection. Across genera, mange-infected canids exhibited reduced microbial diversity, altered community composition and increased abundance of opportunistic pathogens. The primary bacteria comprising secondary infections were Staphylococcus pseudintermedius, previously associated with canid ear and skin infections, and Corynebacterium spp., previously found among the gut flora of S. scabiei mites and hematophagous arthropods.
This evidence suggests that sarcoptic mange infection consistently alters the canid skin microbiome and facilitates secondary bacterial infection, as seen in humans and other mammals infected with S. scabiei mites. These results provide valuable insights into the pathogenesis of mange at the skin barrier of North American canids and can inspire novel treatment strategies. By adopting a "One Health" framework that considers mites, microbes and the potential for interspecies transmission, we can better elucidate the patterns and processes underlying this ubiquitous and enigmatic disease.
Pathogens pose serious threats to human health, agricultural investment, and biodiversity conservation through the emergence of zoonoses, spillover to domestic livestock, and epizootic outbreaks. As ...such, wildlife managers are often tasked with mitigating the negative effects of disease. Yet, parasites form a major component of biodiversity that often persist. This is due to logistical challenges of implementing management strategies and to insufficient understanding of host-parasite dynamics. We advocate for an inclusive understanding of molecular diversity in driving parasite infection and variable host disease states in wildlife systems. More specifically examine the roles of genetic we epigenetic, and commensal microbial variation in disease pathogenesis. These include mechanisms underlying parasite virulence and host resistance and tolerance and the development, regulation, and parasite subversion of immune pathways, among other processes. Case studies of devil facial tumor disease in Tasmanian devils (Sarcophilus harrisii) and chytridiomycosis in globally distributed amphibians exemplify the broad range of questions that can be addressed by examining different facets of molecular diversity. For particularly complex systems integrative molecular analyses present a promising frontier that can provide critical insights necessary to elucidate disease dynamics operating across scales. These insights enable more accurate risk assessment, reconstruction of transmission pathways, discernment of optimal intervention strategies, and development of more effective and ecologically sound treatments that minimize damage to the host Population and environment. Such measures are crucial when m itigating threats posed by wildlife disease to humans, domestic animals and species of conservation concern. Los patógenos presentan amenazas serias para la salud humana, la inversión agrícola, y la conservación de la biodiversidad debido al surgimiento de zoonosis, el paso de estos hacia el ganado doméstico, y los brotes epizoóticos. Por esto manejadores de fauna comúnmente tienen que mitigar los efectos negativos los de las enfermedades. A pesar de esto, los parásitos forman un componente importante de la biodiversidad que generalmente persiste. Esto se debe a los obstáculos logísticas de la implementación de estrategias de manejo y al poco entendimiento de las dinámicas hospedero - parásito. Abogamos por un entendimiento incluyente de la diversidad molecular en la causa de las infecciones parasitarias y los estados variables de los hospederos en sistemas de fauna y examinamos los papeles de la variación microbiana genética, epigenética y comensal en la patogénesis de las enfermedades. Estos papeles incluyen mecanismos subyacentes de la virulencia parasitaria y la resistencia y tolerancia del hospedero, así como el desarrollo, regulación y subversión parasitaria de las vías inmunes, entre otros procesos. Estudios de caso de la enfermedad del tumor facial de los demonios de Tasmania (Sarcophilus harrisii) y la quitridiomicosis en anfibios con distribución mundial ejemplifican la amplia gama de preguntas que pueden abordarse examinando las diferentes facetas de la diversidad molecular. Para sistemas particularmente complejos, los análisis moleculares integrados presentan una frontera prometedora que puede proporcionar conocimiento crítico necesario para elucidar las dinámicas de las enfermedades que operan a lo largo de las escalas. Este conocimiento permite la evaluación más precisa del riesgo, la reconstrucción de las vías de transmisión, el discernimiento de las estrategias óptimas de intervención, y el desarrollo de tratamientos más efectivos y ecológicamente sensatos que minimicen el daño a la población hospedera y al ambiente. Dichas medidas son cruciales cuando se mitigan las amenazas que presentan las enfermedades de fauna silvestre para los humanos, los animales domésticos y las especies de importancia para la conservación. 随着人畜共患病的发生、向家畜中蔓延和动物流行病的爆发，病原体对人类健康、农业投资及生物多祥 性保护都造成了很大的威胁。因而，野生动物管理者时常要负责减轻疾病带来的负面影响。但寄生生物却常常 存在，是生物多祥性的ー个重要组成部分。这将导致管理策略的实施面临挑故，以及对寄主一寄生生物动力学认 识的不足。我们提议要包容性地理解野生生物系统中驱动寄生生物感染和寄主疾病状态变异的分子多祥性，并 研究遗传学、表观遗传学和共生微生物变异在疾病发病机制中的作用。这就要理解寄生生物毒性、寄主抗性 和耐受性的机制，以及在其它过程中免疫通路的发展、调控和受到寄生生物的破坏。我们以袋獾（Sarcopbilus harrisii) 的面部肿瘤病和全球两栖动物的壶菌病为例，证明不同方面的分子多祥性研究可以解决许多问题。对 于特别复杂的系统而言，整合分子生物学分析提供的研究前沿很有希望帮助我们更好地在不同尺度上理解疾病 动力学。这些关键的认识让我们可以更准确地进行风险评估、重建传播途径、找出最优的干预策略，并发展对 寄主种群和环境影响最小、更加有效且环保的处理方法。这样的措施对于减轻野生动物疾病対人类、家养动物 和需要保护的物种的威胁来说至关重要。
The critically endangered black rhinoceros (Diceros bicornis; black rhino) experiences extinction threats from poaching in-situ. The ex-situ population, which serves as a genetic reservoir against ...impending extinction threats, experiences its own threats to survival related to several disease syndromes not typically observed among their wild counterparts. We performed an untargeted metabolomic analysis of serum from 30 ex-situ housed black rhinos (Eastern black rhino, EBR, n = 14 animals; Southern black rhino, SBR, n = 16 animals) and analyzed differences in metabolite profiles between subspecies, sex, and health status (healthy n = 13 vs. diseased n = 14). Of the 636 metabolites detected, several were differentially (fold change > 1.5; p < 0.05) expressed between EBR vs. SBR (40 metabolites), female vs. male (36 metabolites), and healthy vs. diseased (22 metabolites). Results suggest dysregulation of propanoate, amino acid metabolism, and bile acid biosynthesis in the subspecies and sex comparisons. Assessment of healthy versus diseased rhinos indicates involvement of arachidonic acid metabolism, bile acid biosynthesis, and the pentose phosphate pathway in animals exhibiting inflammatory disease syndromes. This study represents the first systematic characterization of the circulating serum metabolome in the black rhinoceros. Findings further implicate mitochondrial and immune dysfunction as key contributors for the diverse disease syndromes reported in ex-situ managed black rhinos.
The host‐associated microbiome is increasingly recognized as a critical player in health and immunity. Recent studies have shown that disruption of commensal microbial communities can contribute to ...disease pathogenesis and severity. Santa Catalina Island foxes (Urocyon littoralis catalinae) present a compelling system in which to examine microbial dynamics in wildlife due to their depauperate genomic structure and extremely high prevalence of ceruminous gland tumors. Although the precise cause is yet unknown, infection with ear mites (Otodectes cynotis) has been linked to chronic inflammation, which is associated with abnormal cell growth and tumor development. Given the paucity of genomic variation in these foxes, other dimensions of molecular diversity, such as commensal microbes, may be critical to host response and disease pathology. We characterized the host‐associated microbiome across six body sites of Santa Catalina Island foxes, and performed differential abundance testing between healthy and mite‐infected ear canals. We found that mite infection was significantly associated with reduced microbial diversity and evenness, with the opportunistic pathogen Staphylococcus pseudintermedius dominating the ear canal community. These results suggest that secondary bacterial infection may contribute to the sustained inflammation associated with tumor development. As the emergence of antibiotic resistant strains remains a concern of the medical, veterinary, and conservation communities, uncovering high relative abundance of S. pseudintermedius provides critical insight into the pathogenesis of this complex system. Through use of culture‐independent sequencing techniques, this study contributes to the broader effort of applying a more inclusive understanding of molecular diversity to questions within wildlife disease ecology.
see also the Perspective by Trevelline et al
Ceruminous gland tumours are highly prevalent in the ear canals of Santa Catalina Island foxes (Urocyon littoralis catalinae). Previous work suggests that tumours may result from a combination of ...ectoparasites, disruption of the host‐associated microbiome, and host immunopathology. More specifically, ear mite infection has been associated with broad‐scale microbial dysbiosis marked by secondary bacterial infection with the opportunistic pathogen Staphylococcus pseudintermedius. Together, ear mites and S. pseudintermedius probably sustain chronic inflammation and promote conditions suitable for tumour development. In the present study, we expanded upon this framework by constructing otic microbial community networks for mite‐infected and uninfected foxes sampled in 2017–2019. Across sampling years, we observed consistent signatures of microbial dysbiosis in mite‐infected ear canals, including reduced microbial diversity and shifted abundance towards S. pseudintermedius. Network analysis further revealed that mite infection disrupts overall community structure. In mite‐infected networks, interaction strengths between taxa were generally weaker, and numerous subnetworks disappeared altogether. We also found that two strains of S. pseudintermedius connected to the main network, suggesting that multistrain biofilm formation may be occurring. In contrast, S. pseudintermedius is peripheral in the uninfected network, with its only connections including a second strain of S. pseudintermedius and the possible competitor Acinetobacter rhizosphaerae. Finally, the lineup of potential keystone taxa shifted across disease states. Fusobacteria spp., a carcinogenesis‐promoting microbe, assumed a keystone role in the mite‐infected community. Considered together, these findings provide insights into how mite infection may destabilize the microbiome and ultimately contribute to tumour development in this island endemic species.
Habitat edge effects can have profound impacts on biodiversity throughout terrestrial and aquatic biomes. Yet, few studies have examined how habitat edge effects impact the spatial patterning of ...sediment properties and microbial communities, especially in coastal ecosystems. Coastal salt marshes throughout the world are being transformed by sea level rise; high-marsh, flood-intolerant species, such as
Spartina patens
, are being fragmented and replaced by low-marsh, flood-tolerant species, such as
Spartina alterniflora.
The consequences of these habitat transformations on fungal communities remain unclear. Thus, we sought to identify how habitat edge effects, alongside changing plant community dynamics, impact the spatial patterning of fungal communities associated with ubiquitous
Spartina
species. We analyzed 26
Spartina patens
patches: 13 pure monocultures and 13 mixed patches with
Spartina alterniflora
infiltration. We measured patch characteristics, plant characteristics, sediment physicochemical properties, and sediment fungal communities. We found that habitat edge effects structured sediment and plant properties in both pure and mixed patches. However, habitat edge effects only structured fungal community composition in mixed patches, counter to expectations. These results indicate that changing plant community dynamics driven by sea level rise can exacerbate habitat edge effects in coastal ecosystems. Least discriminant analysis and co-occurrence networks further revealed unique taxa and network structures between pure and mixed patches and between interiors and edges. In sum, we found that habitat transformation of coastal salt marshes driven by global change impacts the spatial dynamics of sediment and fungal properties.
The host‐associated microbiome is an important player in the ecology and evolution of species. Despite growing interest in the medical, veterinary, and conservation communities, there remain numerous ...questions about the primary factors underlying microbiota, particularly in wildlife. We bridged this knowledge gap by leveraging microbial, genetic, and observational data collected in a wild, pedigreed population of gray wolves (Canis lupus) inhabiting Yellowstone National Park. We characterized body site‐specific microbes across six haired and mucosal body sites (and two fecal samples) using 16S rRNA amplicon sequencing. At the phylum level, we found that the microbiome of gray wolves primarily consists of Actinobacteria, Bacteroidetes, Firmicutes, Fusobacteria, and Proteobacteria, consistent with previous studies within Mammalia and Canidae. At the genus level, we documented body site‐specific microbiota with functions relevant to microenvironment and local physiological processes. We additionally employed observational and RAD sequencing data to examine genetic, demographic, and environmental correlates of skin and gut microbiota. We surveyed individuals across several levels of pedigree relationships, generations, and social groups, and found that social environment (i.e., pack) and genetic relatedness were two primary factors associated with microbial community composition to differing degrees between body sites. We additionally reported body condition and coat color as secondary factors underlying gut and skin microbiomes, respectively. We concluded that gray wolf microbiota resemble similar host species, differ between body sites, and are shaped by numerous endogenous and exogenous factors. These results provide baseline information for this long‐term study population and yield important insights into the evolutionary history, ecology, and conservation of wild wolves and their associated microbes.
We characterized the host‐associated microbiome across multiple body sites in gray wolves living in Yellowstone National Park, USA. Leveraging genetic, microbial, and observational data, we determined that social environment and genetics primarily underly microbial community composition in this wild mammalian system. Photo credit: NPS/Jacob W. Frank, Jim Peaco, and Daniel Stahler.
Environmental variation can influence the reproductive success of species managed under human care and in the wild, yet the mechanisms underlying this phenomenon remain largely mysterious. Molecular ...mechanisms such as epigenetic modifiers are important in mediating the timing and progression of reproduction in humans and model organisms, but few studies have linked epigenetic variation to reproductive fitness in wildlife. Here, we investigated epigenetic variation in black‐footed ferrets (Mustela nigripes), an endangered North American mammal reliant on ex situ management for survival and persistence in the wild. Despite similar levels of genetic diversity in human‐managed and wild‐born populations, individuals in ex situ facilities exhibit reproductive problems, such as poor sperm quality. Differences across these settings suggest that an environmentally driven decline in reproductive capacity may be occurring in this species. We examined the role of DNA methylation, one well‐studied epigenetic modifier, in this emergent condition. We leveraged blood, testes, and semen samples from male black‐footed ferrets bred in ex situ facilities and found tissue‐type specificity in DNA methylation across the genome, although 1360 Gene Ontology terms associated with male average litter size shared functions across tissues. We then constructed gene networks of differentially methylated genomic sites associated with three different reproductive phenotypes to explore the putative biological impact of variation in DNA methylation. Sperm gene networks associated with average litter size and sperm count were functionally enriched for candidate genes involved in reproduction, development, and its regulation through transcriptional repression. We propose that DNA methylation plays an important role in regulating these reproductive phenotypes, thereby impacting the fertility of male ex situ individuals. Our results provide information into how DNA methylation may function in the alteration of reproductive pathways and phenotypes in artificial environments. These findings provide early insights to conservation hurdles faced in the protection of this rare species.
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
The gut microbiome of mammals engages in a dynamic relationship with the body and contributes to numerous physiological processes integral to overall health. Understanding the factors ...shaping animal-associated bacterial communities is therefore paramount to the maintenance and management in ex situ wildlife populations. Here, we characterized the gut microbiome of 48 endangered black-footed ferrets (Mustela nigripes) housed at Smithsonian’s National Zoo and Conservation Biology Institute (Front Royal, Virginia, USA). We collected longitudinal fecal samples from males and females across two distinct reproductive seasons to consider the role of host sex and reproductive physiology in shaping bacterial communities, as measured using 16S rRNA amplicon sequencing. Within each sex, gut microbial composition differed between breeding and non-breeding seasons, with five bacterial taxa emerging as differentially abundant. Between sexes, female and male microbiomes were similar during non-breeding season but significantly different during breeding season, which may result from sex-specific physiological changes associated with breeding. Finally, we found low overall diversity consistent with other mammalian carnivores alongside high relative abundances of potentially pathogenic microbes such as Clostridium, Escherichia, Paeniclostridium, and (to a lesser degree) Enterococcus—all of which have been associated with gastrointestinal or reproductive distress in mammalian hosts, including black-footed ferrets. We recommend further study of these microbes and possible therapeutic interventions to promote more balanced microbial communities. These results have important implications for ex situ management practices that can improve the gut microbial health and long-term viability of black-footed ferrets.
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