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The putatively positive association between host genetic diversity and the ability to defend against pathogens has long attracted the attention of evolutionary biologists. Chytridiomycosis, a disease caused by the chytrid fungus Batrachochytrium dendrobatidis (Bd), has emerged in recent decades as a cause of dramatic declines and extinctions across the amphibian clade. Bd susceptibility can vary widely across populations of the same species, but the relationship between standing genetic diversity and susceptibility has remained notably underexplored so far. Here, we focus on a putatively Bd-naive system of two mainland and two island populations of the common toad (Bufo bufo) at the edge of the species’ range, and use controlled infection experiments and dd-RAD sequencing of >10,000 SNPs across 95 individuals to characterise the role of host population identity, genetic variation and individual body mass in mediating host response to the pathogen. We found strong genetic differentiation between populations and marked variation in their susceptibility to Bd. This variation was not, however, governed by isolation-mediated genetic erosion, and individual heterozygosity was even found to be negatively correlated with survival. Individual survival during infection experiments was strongly positively related to body mass, which itself was unrelated to population of origin or heterozygosity. Our findings underscore the general importance of context-dependency when assessing the role of host genetic variation for the ability of defence against pathogens.

The global trend of increasing environmental temperatures is often predicted to result in more severe disease epidemics. However, unambiguous evidence that temperature is a driver of epidemics is largely lacking, because it is demanding to demonstrate its role among the complex interactions between hosts, pathogens, and their shared environment. Here, we apply a three-pronged approach to understand the effects of temperature on ranavirus epidemics in UK common frogs, combining in vitro, in vivo, and field studies. Each approach suggests that higher temperatures drive increasing severity of epidemics. In wild populations, ranavirosis incidents were more frequent and more severe at higher temperatures, and their frequency increased through a period of historic warming in the 1990s. Laboratory experiments using cell culture and whole animal models showed that higher temperature increased ranavirus propagation, disease incidence, and mortality rate. These results, combined with climate projections, predict severe ranavirosis outbreaks will occur over wider areas and an extended season, possibly affecting larval recruitment. Since ranaviruses affect a variety of ectothermic hosts (amphibians, reptiles, and fish), wider ecological damage could occur. Our three complementary lines of evidence present a clear case for direct environmental modulation of these epidemics and suggest management options to protect species from disease.

Variation among animals in their host-associated microbial communities is increasingly recognized as a key determinant of important life history traits including growth, metabolism, and resistance to disease. Quantitative estimates of the factors shaping the stability of host microbiomes over time at the individual level in non-model organisms are scarce. Addressing this gap in our knowledge is important, as variation among individuals in microbiome stability may represent temporal gain or loss of key microbial species and functions linked to host health and/or fitness. Here we use controlled experiments to investigate how both heterogeneity in microbial species richness of the environment and exposure to the emerging pathogen Ranavirus influence the structure and temporal dynamics of the skin microbiome in a vertebrate host, the European common frog (Rana temporaria). Our evidence suggests that altering the bacterial species richness of the environment drives divergent temporal microbiome dynamics of the amphibian skin. Exposure to ranavirus effects changes in skin microbiome structure irrespective of total microbial diversity, but individuals with higher pre-exposure skin microbiome diversity appeared to exhibit higher survival. Higher diversity skin microbiomes also appear less stable over time compared to lower diversity microbiomes, but stability of the 100 most abundant (“core”) community members was similar irrespective of microbiome richness. Our study highlights the importance of extrinsic factors in determining the stability of host microbiomes over time, which may in turn have important consequences for the stability of host-microbe interactions and microbiome-fitness correlations.

Ranavirus is the second most common infectious cause of amphibian mortality. These viruses affect caudates, an order in which information regarding Ranavirus pathogenesis is scarce. In the Netherlands, two strains (CMTV-NL I and III) were suspected to possess distinct pathogenicity based on field data. To investigate susceptibility and disease progression in urodeles and determine differences in pathogenicity between strains, 45 adult smooth newts (Lissotriton vulgaris) were challenged via bath exposure with these ranaviruses and their detection in organs and feces followed over time by PCR, immunohistochemistry and in situ hybridization. Ranavirus was first detected at 3 days post infection (p.i.) in the oral cavity and upper respiratory mucosa. At 6 days p.i, virus was found in connective tissues and vasculature of the gastrointestinal tract. Finally, from 9 days p.i onwards there was widespread Ranavirus disease in various organs including skin, kidneys and gonads. Higher pathogenicity of the CMTV-NL I strain was confirmed by higher correlation coefficient of experimental group and mortality of challenged animals. Ranavirus-exposed smooth newts shed virus in feces intermittently and infection was seen in the absence of lesions or clinical signs, indicating that this species can harbor subclinical infections and potentially serve as disease reservoirs.

Increasing environmental temperatures are predicted to have increasingly severe and deleterious effects on biodiversity. For the most part, the impacts of a warming environment are presumed to be direct, however some predict increasingly severe disease epidemics, primarily from vector-borne pathogens, that will have the capacity to deplete host populations. Data to support this hypothesis are lacking. Here we describe increasing severity of ranavirosis driven by increasing temperature affecting a widely distributed amphibian host. Both in vitro and in vivo experiments showed that increasing environmental temperature leads to increased propagation of ranavirus and, in the latter, increased incidence of host infection and mortality. Also, temperature was shown to be a key determinant of disease dynamics in wild amphibians, raising the odds and severity of disease incidents. The direction of this effect was highly consistent in the context of other interacting variables such as shading around ponds. Projections based on future climate indicate that changes in seasonal weather in the UK will result in the increased incidence of severe cases of ranavirosis in amphibian populations that could affect recruitment. These complementary lines of evidence present a clear case of direct environmental modulation of a host-pathogen interaction and provide information for proposing mitigation actions.

Environmental heterogeneity is known to modulate the interactions between pathogens and hosts. However, the impact of environmental heterogeneity on the structure of host-associated microbial communities, and how these communities respond to pathogenic exposure remain poorly understood. Here we use an experimental framework to probe the links between environmental heterogeneity, skin microbiome structure and infection by the emerging pathogenRanavirusin a vertebrate host, the European common frog (Rana temporaria). We provide evidence that environmental complexity directly influences the diversity and structure of the host skin microbiome, and that more diverse microbiomes are more resistant to perturbation associated with exposure toRanavirus. Our data also indicate that host microbiome diversity covaries with survival following exposure toRanavirus. Our study highlights the importance of extrinsic factors in driving host-pathogen dynamics in vertebrate hosts, and suggests that environment-mediated variation in the structure of the host microbiome may covary with observed differences in host susceptibility to disease in the wild.