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BackgroundAmphibians are experiencing substantial declines attributed to emerging pathogens. Efforts to understand what drives patterns of pathogen prevalence and differential responses among species are challenging because numerous factors related to the host, pathogen, and their shared environment can influence infection dynamics. Furthermore, sampling across broad taxonomic and geographic scales to evaluate these factors poses logistical challenges, and interpreting the roles of multiple potentially correlated variables is difficult with traditional statistical approaches. In this study, we leverage frozen tissues stored in natural history collections and machine learning techniques to characterize infection dynamics of three generalist pathogens known to cause mortality in frogs. MethodsWe selected 12 widespread and abundant focal taxa within three ecologically distinct, co-distributed host families (Bufonidae, Hylidae, and Ranidae) and sampled them across the eastern two-thirds of the United States of America. We screened and quantified infection loadsviaquantitative PCR for three major pathogens: the fungal pathogenBatrachochytrium dendrobatidis(Bd), double-stranded viruses in the lineageRanavirus(Rv), and the alveolate parasite currently referred to as Amphibian Perkinsea (Pr). We then built balanced random forests (RF) models to predict infection status and intensity based on host taxonomy, age, sex, geography, and environmental variables and to assess relative variable importance across pathogens. Lastly, we used one-way analyses to determine directional relationships and significance of identified predictors. ResultsWe found approximately 20% of individuals were infected with at least one pathogen (231 single infections and 25 coinfections). The most prevalent pathogen across all taxonomic groups was Bd (16.9%; 95% CI [14.9–19%]), followed by Rv (4.38%; 95% CI [3.35–5.7%]) and Pr (1.06%; 95% CI [0.618–1.82%]). The highest prevalence and intensity were found in the family Ranidae, which represented 74.3% of all infections, including the majority of Rv infection points, and had significantly higher Bd intensities compared to Bufonidae and Hylidae. Host species and environmental variables related to temperature were key predictors identified in RF models, with differences in importance among pathogens and host families. For Bd and Rv, infected individuals were associated with higher latitudes and cooler, more stable temperatures, while Pr showed trends in the opposite direction. We found no significant differences between sexes, but juvenile frogs had higher Rv prevalence and Bd infection intensity compared to adults. Overall, our study highlights the use of machine learning techniques and a broad sampling strategy for identifying important factors related to infection in multi-host, multi-pathogen systems. 

ABSTRACT Anthropogenic habitat disturbance is fundamentally altering patterns of disease transmission and immunity across the vertebrate tree of life. Most studies linking anthropogenic habitat change and disease focus on habitat loss and fragmentation, but these processes often lead to a third process that is equally important:habitat split. Defined as spatial separation between the multiple classes of natural habitat that many vertebrate species require to complete their life cycles, habitat split has been linked to population declines in vertebrates, e.g. amphibians breeding in lowland aquatic habitats and overwintering in fragments of upland terrestrial vegetation. Here, we link habitat split to enhanced disease risk in amphibians (i) by reviewing the biotic and abiotic forces shaping elements of immunity and (ii) through a spatially oriented field study focused on tropical frogs. We propose a framework to investigate mechanisms by which habitat split influences disease risk in amphibians, focusing on three broad host factors linked to immunity: (i) composition of symbiotic microbial communities, (ii) immunogenetic variation, and (iii) stress hormone levels. Our review highlights the potential for habitat split to contribute to host‐associated microbiome dysbiosis, reductions in immunogenetic repertoire, and chronic stress, that often facilitate pathogenic infections and disease in amphibians and other classes of vertebrates. We highlight that targeted habitat‐restoration strategies aiming to connect multiple classes of natural habitats (e.g. terrestrial–freshwater, terrestrial–marine, marine–freshwater) could enhance priming of the vertebrate immune system through repeated low‐load exposure to enzootic pathogens and reduced stress‐induced immunosuppression.