Ranaviruses are pathogens associated with the decline of amphibian populations across much of their distribution. In North America, frog virus 3 (FV3) is a widely distributed pathogen with wild populations of amphibians harboring different lineages and putative recombinants between FV3 and common midwife toad virus (CMTV). These recombinants have higher pathogenicity, and CMTV-derived genes associated with virulence are reported in wild strains in Canada. However, while FV3 is linked to amphibian die-offs in North America, CMTVs have been reported only in commercial frog farms in North America. We sequenced complete genomes of 18 FV3 isolates from three amphibian species to characterize genetic diversity of the lineages in Canada and infer possible recombinant regions. The 18 FV3 isolates displayed different signals of recombination, varying from none to interspersed recombination with previously isolated CMTV-like viruses. In general, most recombination breakpoints were located within open reading frames (ORFs), generating new ORFs and proteins that were a mixture between FV3 and CMTV. A combined spatial and temporal phylogeny suggests the presence of the FV3 lineage in Canada is relatively contemporary (<100 years), corroborating the hypothesis that both CMTV- and FV3-like viruses spread to North America when the international commercial amphibian trade started. Our results highlight the importance of pathogen surveillance and viral dynamics using full genomes to more clearly understand the mechanisms of disease origin and spread. IMPORTANCE Amphibian populations are declining worldwide, and these declines have been linked to a number of anthropogenic factors, including disease. Among the pathogens associated with amphibian mortality, ranaviruses have caused massive die-offs across continents. In North America, frog virus 3 (FV3) is a widespread ranavirus that can infect wild and captive amphibians. In this study, we sequenced full FV3 genomes isolated from frogs in Canada. We report widespread recombination between FV3 and common midwife toad virus (CMTV). Phylogenies indicate a recent origin for FV3 in Canada, possibly as a result of international amphibian trade.
Pathogen-induced population declines and extinction events have been recognized as main threats to amphibian species around the globe. However, the ecological drivers underlying epidemiological patterns are still poorly understood. In an attempt to assess the current knowledge on the ecological drivers of amphibian diseases, we identified 832 peer-reviewed publications on the ecology of amphibian pathogens and diseases published between 2009 and 2019. The vast majority of publications investigated either chytrid or ranavirus infections (79% of the articles), whereas other pathogens such as bacteria and helminths received considerably less attention. Just over half of the studies we reviewed included field research and 40% were experimental in nature, yet only 8% combined field and experimental approaches. More than half of the literature (56%) investigated postmetamorphic stages, whereas premetamorphic stages were considered in 23% of the reviewed studies, and only 13% included both life stages. Susceptibility and mortality have been assessed in almost every study (91%) whereas 37% of them tested for cellular, physiological, or immunological responses. However, other host characteristics such as growth/development, behavior, and specific mucosome/microbiome were considered in only one of four studies. Most research included at least one biotic factor (e.g., host and pathogen identity, species diversity, genetic adaptations), but only one-third considered environmental factors (e.g., temperature, landscape features, inorganic chemicals). Furthermore, there is no general consensus about the factors driving epidemiological patterns of pathogens in amphibian communities, and it is clear that the complexity and specificity of interactions between ecological factors and host-pathogen dynamics make conservation implications difficult and management decisions challenging. To this end, our review identifies some research gaps and proposes future directions to better understand one of the major threats to this class of vertebrates.
In an era where emerging infectious diseases are a serious threat to biodiversity, epidemiological patterns need to be identified, particularly the complex mechanisms driving the dynamics of multi-host pathogens in natural communities. Many amphibian species have faced unprecedented population declines associated with diseases. Yet, specific processes shaping host-pathogen relationships within and among communities for amphibian pathogens such as ranaviruses (RV) remain poorly understood. To address this gap, we conducted a comprehensive study of RV in low-diversity amphibian communities in north-western Canada to assess the effects of biotic factors (species identity, species richness, abundance) and abiotic factors (conductivity, pH) on the pathogen prevalence and viral loads. Across 2 years and 18 sites, with communities of up to three hosts (wood frog, Rana sylvatica; boreal chorus frog, Pseudacris maculata; Canadian toad, Anaxyrus hemiophrys), we observed that RV prevalence nearly doubled with each additional species in a community, suggesting an amplification effect in aquatic, as well as terrestrial life-history stages. Infection intensity among infected wood frogs and boreal chorus frogs also significantly increased with an increase in species richness. Interestingly, we did not observe any effects of host abundance or abiotic factors, highlighting the importance of including host identity and species richness when investigating multi-host pathogens. Ultimately, only such a comprehensive approach can improve our understanding of complex and often highly context-dependent host-pathogen interactions.
Investigation of mortalities in isolated wild amphibian populations presents diagnostic difficulties that can hinder reaching a definitive diagnosis for the cause of death. Disease can only be diagnosed when pathogen presence (e.g. detection by PCR) is linked to tissue lesions (histopathology) in the host. We report a 2-site outbreak of ranavirosis in wild anuran tadpoles in the boreal forest of Wood Buffalo National Park, Canada, diagnosed by histologic and molecular techniques. Mortalities occurred in wood frog Rana sylvatica tadpoles and boreal chorus frog Pseudacris maculata tadpoles. Lack of mortality in sympatric Canadian toad Bufo (Anaxyrus) hemiophrys tadpoles suggested lower disease susceptibility in this species. In the former 2 species, ranavirosis was diagnosed based on consistent histopathology, immunohistochemistry (IHC), in situ hybridization (ISH), and quantitative PCR results. The most common histopathologic lesion present in wood and boreal chorus frog tadpoles was necrosis of the skin, oral mucosa, renal tubular epithelium, renal hematopoietic tissue, and branchial epithelium. Mild hepatic and pancreatic necrosis and rare intracytoplasmic inclusion bodies in hepatocytes were less common. Skeletal and connective tissues in budding limbs often had multifocal to coalescing necrosis and were intensely positive for ranavirus, with IHC staining even in areas where no obvious necrosis could be observed. Abundant IHC and ISH staining in actively growing tissues support a link between disease emergence and amphibian developmental stage. Our findings provide a definitive diagnosis of ranavirosis in free-living amphibians and highlight the effectiveness of multi-tool approaches to mortality investigation and elucidation of pathogenesis of ranavirosis in wild amphibians.
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