The past two decades have seen an increasing number of virulent infectious diseases in natural populations and managed landscapes. In both animals and plants, an unprecedented number of fungal and fungal-like diseases have recently caused some of the most severe die-offs and extinctions ever witnessed in wild species, and are jeopardizing food security. Human activity is intensifying fungal disease dispersal by modifying natural environments and thus creating new opportunities for evolution. We argue that nascent fungal infections will cause increasing attrition of biodiversity, with wider implications for human and ecosystem health, unless steps are taken to tighten biosecurity worldwide.

Epidemiological theory generally suggests that pathogens will not cause host extinctions because the pathogen should fade out when the host population is driven below some threshold density. An emerging infectious disease, chytridiomycosis, caused by the fungal pathogen Batrachochytrium dendrobatidis (Bd) is directly linked to the recent extinction or serious decline of hundreds of amphibian species. Despite continued spread of this pathogen into uninfected areas, the dynamics of the host-pathogen interaction remain unknown. We use fine-scale spatiotemporal data to describe (i) the invasion and spread of Bd through three lake basins, each containing multiple populations of the mountain yellow-legged frog, and (ii) the accompanying host-pathogen dynamics. Despite intensive sampling, Bd was not detected on frogs in study basins until just before epidemics began. Following Bd arrival in a basin, the disease spread to neighboring populations at ≈700 m/yr in a wave-like pattern until all populations were infected. Within a population, infection prevalence rapidly reached 100% and infection intensity on individual frogs increased in parallel. Frog mass mortality began only when infection intensity reached a critical threshold and repeatedly led to extinction of populations. Our results indicate that the high growth rate and virulence of Bd allow the nearsimultaneous infection and buildup of high infection intensities in all host individuals; subsequent host population crashes therefore occur before Bd is limited by density-dependent factors. Preventing infection intensities in host populations from reaching this threshold could provide an effective strategy to avoid the extinction of susceptible amphibian species in the wild.amphibian declines | Batrachochytrium dendrobatidis | chytridiomycosis | emerging infectious disease | Rana muscosa E arth's biodiversity is increasingly threatened with extinction.

Chytridiomycosis, the disease caused by the chytrid fungus, Batrachochytrium dendrobatidis (Bd), has contributed to amphibian population declines and extinctions worldwide. The impact of this pathogen, however, varies markedly among amphibian species and populations. Following invasion into some areas of California's Sierra Nevada, Bd leads to rapid declines and local extinctions of frog populations ( Rana muscosa , R. sierrae ). In other areas, infected populations of the same frog species have declined but persisted at low host densities for many years. We present results of a 5-year study showing that infected adult frogs in persistent populations have low fungal loads, are surviving between years, and frequently lose and regain the infection. Here we put forward the hypothesis that fungal load dynamics can explain the different population-level outcomes of Bd observed in different areas of the Sierra Nevada and possibly throughout the world. We develop a model that incorporates the biological details of the Bd-host interaction. Importantly, model results suggest that host persistence versus extinction does not require differences in host susceptibility, pathogen virulence, or environmental conditions, and may be just epidemic and endemic population dynamics of the same host–pathogen system. The different disease outcomes seen in natural populations may result solely from density-dependent host–pathogen dynamics. The model also shows that persistence of Bd is enhanced by the long-lived tadpole stage that characterize these two frog species, and by nonhost Bd reservoirs.

Emerging infectious diseases threaten human and wildlife populations. Altered ecological interactions between mutualistic microbes and hosts can result in disease, but an understanding of interactions between host, microbes and disease-causing organisms may lead to management strategies to affect disease outcomes. Many amphibian species in relatively pristine habitats are experiencing dramatic population declines and extinctions due to the skin disease chytridiomycosis, which is caused by the chytrid fungus Batrachochytrium dendrobatidis. Using a randomized, replicated experiment, we show that adding an antifungal bacterial species, Janthinobacterium lividum, found on several species of amphibians to the skins of the frog Rana muscosa prevented morbidity and mortality caused by the pathogen. The bacterial species produces the anti-chytrid metabolite violacein, which was found in much higher concentrations on frog skins in the treatments where J. lividum was added. Our results show that cutaneous microbes are a part of amphibians' innate immune system, the microbial community structure on frog skins is a determinant of disease outcome and altering microbial interactions on frog skins can prevent a lethal disease outcome. A bioaugmentation strategy may be an effective management tool to control chytridiomycosis in amphibian survival assurance colonies and in nature.

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Understanding the evolutionary history of microbial pathogens is critical for mitigating the impacts of emerging infectious diseases on economically and ecologically important host species. We used a genome resequencing approach to resolve the evolutionary history of an important microbial pathogen, the chytrid Batrachochytrium dendrobatidis (Bd), which has been implicated in amphibian declines worldwide. We sequenced the genomes of 29 isolates of Bd from around the world, with an emphasis on North, Central, and South America because of the devastating effect that Bd has had on amphibian populations in the New World. We found a substantial amount of evolutionary complexity in Bd with deep phylogenetic diversity that predates observed global amphibian declines. By investigating the entire genome, we found that even the most recently evolved Bd clade (termed the global panzootic lineage) contained more genetic variation than previously reported. We also found dramatic differences among isolates and among genomic regions in chromosomal copy number and patterns of heterozygosity, suggesting complex and heterogeneous genome dynamics. Finally, we report evidence for selection acting on the Bd genome, supporting the hypothesis that protease genes are important in evolutionary transitions in this group. Bd is considered an emerging pathogen because of its recent effects on amphibians, but our data indicate that it has a complex evolutionary history that predates recent disease outbreaks. Therefore, it is important to consider the contemporary effects of Bd in a broader evolutionary context and identify specific mechanisms that may have led to shifts in virulence in this system.

Significance Animals are inhabited by communities of microbes (the microbiome) that potentially interact with pathogens. Detailed studies of microbiome–pathogen interactions in nature are rare, and even when correlations are observed, determining causal relationships is challenging. The microbiome–pathogen relationship is of particular interest in the case of Batrachochytrium dendrobatidis , a chytrid fungus that infects the skin of amphibians and is causing amphibian declines worldwide. We documented a strong correlation between pathogen load and skin bacterial communities of frogs during natural disease episodes. We then showed experimentally that infection alters the microbiome, with similar bacteria responding in both laboratory and field. The results indicate that the chytrid pathogen drives changes in the amphibian skin microbiome during disease episodes in wild frogs.

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