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ImportanceInherent complexities in the composition of microbiomes can often preclude investigations of microbe-associated diseases. Instead of single organisms being associated with disease, community characteristics may be more relevant. Longitudinal microbiome studies of the same individual bats as pathogens arrive and infect a population are the ideal experiment but remain logistically challenging; therefore, investigations like our approach that are able to correlate invasive pathogens to alterations within a microbiome may be the next best alternative. The results of this study potentially suggest that microbiome-host interactions may determine the likelihood of infection. However, the contrasting relationship between Pd and the bacterial microbiomes of Myotis lucifugus and Perimyotis subflavus indicate that we are just beginning to understand how the bat microbiome interacts with a fungal invader such as Pd.

Demographic factors are fundamental in shaping infectious disease dynamics. Aspects of populations that create structure, like age and sex, can affect patterns of transmission, infection intensity and population outcomes. However, studies rarely link these processes from individual to population-scale effects. Moreover, the mechanisms underlying demographic differences in disease are frequently unclear. Here, we explore sex-biased infections for a multi-host fungal disease of bats, white-nose syndrome, and link disease-associated mortality between sexes, the distortion of sex ratios and the potential mechanisms underlying sex differences in infection. We collected data on host traits, infection intensity and survival of five bat species at 42 sites across seven years. We found females were more infected than males for all five species. Females also had lower apparent survival over winter and accounted for a smaller proportion of populations over time. Notably, female-biased infections were evident by early hibernation and likely driven by sex-based differences in autumn mating behaviour. Male bats were more active during autumn which likely reduced replication of the cool-growing fungus. Higher disease impacts in female bats may have cascading effects on bat populations beyond the hibernation season by limiting recruitment and increasing the risk of Allee effects.

Disease results from interactions among the host, pathogen, and environment. Inoculation trials can quantify interactions among these players and explain aspects of disease ecology to inform management in variable and dynamic natural environments. White-nose Syndrome, a disease caused by the fungal pathogen, Pseudogymnoascus destructans (Pd), has caused severe population declines of several bat species in North America. We conducted the first experimental infection trial on the tri-colored bat, Perimyotis subflavus, to test the effect of temperature and humidity on disease severity. We also tested the effects of temperature and humidity on fungal growth and persistence on substrates. Unexpectedly, only 37% (35/95) of bats experimentally inoculated with Pd at the start of the experiment showed any infection response or disease symptoms after 83 days of captive hibernation. There was no evidence that temperature or humidity influenced infection response. Temperature had a strong effect on fungal growth on media plates, but the influence of humidity was more variable and uncertain. Designing laboratory studies to maximize research outcomes would be beneficial given the high costs of such efforts and potential for unexpected outcomes. Understanding the influence of microclimates on host-pathogen interactions remains an important consideration for managing wildlife diseases, particularly in variable environments.

Disease outbreaks and pathogen introductions can have significant effects on host populations, and the ability of pathogens to persist in the environment can exacerbate disease impacts by fueling sustained transmission, seasonal epidemics, and repeated spillover events. While theory suggests that the presence of an environmental reservoir increases the risk of host declines and threat of extinction, the influence of reservoir dynamics on transmission and population impacts remains poorly described. Here we show that the extent of the environmental reservoir explains broad patterns of host infection and the severity of disease impacts of a virulent pathogen. We examined reservoir and host infection dynamics and the resulting impacts of Pseudogymnoascus destructans, the fungal pathogen that causes white-nose syndrome, in 39 species of bats at 101 sites across the globe. Lower levels of pathogen in the environment consistently corresponded to delayed infection of hosts, fewer and less severe infections, and reduced population impacts. In contrast, an extensive and persistent environmental reservoir led to early and widespread infections and severe population declines. These results suggest that continental differences in the persistence or decay of P. destructans in the environment altered infection patterns in bats and influenced whether host populations were stable or experienced severe declines from this disease. Quantifying the impact of the environmental reservoir on disease dynamics can provide specific targets for reducing pathogen levels in the environment to prevent or control future epidemics.

Tools for reducing wildlife disease impacts are needed to conserve biodiversity. White-nose syndrome (WNS), caused by the fungus Pseudogymnoascus destructans, has caused widespread declines in North American bat populations and threatens several species with extinction. Few tools exist for managers to reduce WNS impacts. We tested the efficacy of a probiotic bacterium, Pseudomonas fluorescens, to reduce impacts of WNS in two simultaneous experiments with caged and free-flying Myotis lucifugus bats at a mine in Wisconsin, USA. In the cage experiment there was no difference in survival between control and P. fluorescens-treated bats. However, body mass, not infection intensity, predicted mortality, suggesting that within-cage disturbance influenced the cage experiment. In the free-flying experiment, where bats were able to avoid conspecific disturbance, infection intensity predicted the date of emergence from the mine. In this experiment treatment with P. fluorescens increased apparent overwinter survival five-fold compared to the control group (from 8.4% to 46.2%) by delaying emergence of bats from the site by approximately 32 days. These results suggest that treatment of bats with P. fluorescens may substantially reduce WNS mortality, and, if used in combination with other interventions, could stop population declines.

Anthropogenically driven environmental change has imposed substantial threats on biodiversity, including the emergence of infectious diseases that have resulted in declines of wildlife globally. In response to pathogen invasion, maintaining diversity within host populations across heterogenous environments is essential to facilitating species persistence. White-nose syndrome is an emerging fungal pathogen that has caused mass mortalities of hibernating bats across North America. However, in the northeast, peripheral island populations of the endangered northern myotis (Myotis septentrionalis) appear to be persisting despite infection while mainland populations in the core of the species range have experienced sharp declines. Thus, this study investigated host and environmental factors that may contribute to divergent population responses. We compared patterns of pathogen exposure and infection intensity between populations and documented the environmental conditions and host activity patterns that may promote survival despite disease invasion. For island populations, we found lower prevalence and less severe infections, possibly due to a shorter hibernation duration compared to the mainland, which may reduce the time for disease progression. The coastal region of the northern myotis range may serve as habitat refugia that enables this species to persist despite pathogen exposure; however, conservation efforts could be critical to supporting species survival in the long term. [ABSTRACT FROM AUTHOR]

Background: Potentially zoonotic pathogens have been previously detected in bat-associated ticks, but their role in disease transmission and their frequency of feeding on non-bat hosts is poorly known. Methodology/Principal findings: We used molecular blood meal analysis to reveal feeding patterns of the bat-associated tick species Ixodes ariadnae, I. simplex, and I. vespertilionis collected from cave and mine walls in Central and Southeastern Europe. Vertebrate DNA, predominantly from bats, was detected in 43.5% of the samples (70 of 161 ticks) but in these ticks we also detected the DNA of non-chiropteran hosts, such as dog, Canis lupus familiaris, wild boar, Sus scrofa, and horse, Equus caballus, suggesting that bat-associated ticks may exhibit a much broader host range than previously thought, including domestic and wild mammals. Furthermore, we detected the zoonotic bacteria Neoehrlichia mikurensis in bat ticks for the first time, and other bacteria, such as Bartonella and Wolbachia. Conclusions/Significance: In the light of these findings, the role of bat ticks as disease vectors should be urgently re-evaluated in more diverse host systems, as they may contribute to pathogen transmission between bats and non-chiropteran hosts. Author summary: Ticks found on bats might carry diseases that can be important for both animal and human health. In this study we collected three species of bat ticks and used molecular methods to demonstrate their feeding habits and to explore the pathogens they carry. We found that most of the ticks had been feeding on bats, but we also found evidence of blood meals from domestic and wild animals, such as dogs, wild boars, and horses. We also found several bacteria in these ticks that can infect or potentially infect humans and animals. These results indicate that bat ticks could be a potential link between bats and non-bat hosts and may help spread diseases between them. Learning about how ticks interact with different host species is critical to understanding the ecology and spread of wildlife disease. [ABSTRACT FROM AUTHOR]

Soft ticks in the genus Ornithodoros occur throughout the Mojave Desert in southern Nevada, southeastern California, and parts of southwestern Utah and northwestern Arizona, USA, and are frequently observed parasitizing Mojave desert tortoises (Gopherus agassizii). However, limited research exists examining the relationship between ticks and desert tortoises. Mojave desert tortoises are listed as threatened by the US Fish and Wildlife Service, and as such, their populations are monitored and individual tortoise health is routinely assessed. These health assessments document the presence and abundance of ticks present on tortoises, but detailed examination of the relationship between ticks and tortoise health has been lacking. This study analyzed the relationship between tick presence and desert tortoise health assessments as a function of season, location, age (adult vs. juvenile), foraging behavior, evidence of clinical signs of disease, body condition score, and sex. Our results indicate that more ticks were found on tortoises in the summer than in any other season. Ticks were observed more frequently on captive tortoises versus wild tortoises, and more ticks were likely to be present on adult tortoises than on juveniles. Ticks were also more likely to be observed on tortoises that lacked evidence of foraging and on tortoises with observed clinical signs of disease. These findings provide valuable insights into the biology of ticks in relation to tortoises that may be useful for management of both captive and free-living threatened tortoise populations where ticks are detected. Our study also may improve understanding of potential tick-borne disease dynamics in the Mojave desert tortoise habitat, including Borrelia sp. carried by Ornithodoros ticks, which cause tick- borne relapsing fever in people. [ABSTRACT FROM AUTHOR]

The animal gut microbiome can have a strong influence on the health, fitness, and behavior of its hosts. The composition of the gut microbial community can be influenced by factors such as diet, environment, and evolutionary history (phylosymbiosis). However, the relative influence of these factors is unknown in most bird species. Furthermore, phylosymbiosis studies have largely focused on clades that diverged tens of millions of years ago, and little is known about the degree of gut microbiome divergence in more recent species radiations. This study explores the drivers of microbiome variation across the unique and recent Hawaiian honeycreeper radiation (Fringillidae: Drepanidinae). Fecal samples were collected from 14 extant species spanning the main islands of the Hawaiian archipelago and were sequenced using three metabarcoding markers to characterize the gut microbiome, invertebrate diet, and plant diet of Hawaiian honeycreepers. We then used these metabarcoding data and the honeycreeper host phylogeny to evaluate their relative roles in shaping the gut microbiome. Microbiome variation across birds was highly individualized; however, source island had a small but significant effect on microbiome structure. The microbiomes did not recapitulate the host phylogenetic tree, indicating that evolutionary history does not strongly influence microbiome structure in the honeycreeper clade. These results expand our understanding of the roles of diet, geography, and phylogeny on avian microbiome structure, while also providing important ecological information about the diet and gut microbiota of wild Hawaiian honeycreepers. [ABSTRACT FROM AUTHOR]

Predicting species' fates following the introduction of a novel pathogen is a significant and growing problem in conservation. Comparing disease dynamics between introduced and endemic regions can offer insight into which naive hosts will persist or go extinct, with disease acting as a filter on host communities. We examined four hypothesized mechanisms for host-pathogen persistence by comparing host infection patterns and environmental reservoirs for Pseudogymnoascus destructans (the causative agent of white-nose syndrome) in Asia, an endemic region, and North America, where the pathogen has recently invaded. Although colony sizes of bats and hibernacula temperatures were very similar, both infection prevalence and fungal loads were much lower on bats and in the environment in Asia than North America. These results indicate that transmission intensity and pathogen growth are lower in Asia, likely due to higher host resistance to pathogen growth in this endemic region, and not due to host tolerance, lower transmission due to smaller populations, or lower environmentally driven pathogen growth rate. Disease filtering also appears to be favouring initially resistant species in North America. More broadly, determining the mechanisms allowing species persistence in endemic regions can help identify species at greater risk of extinction in introduced regions, and determine the consequences for disease dynamics and host-pathogen coevolution.

White-nose syndrome has devastated bat populations in eastern North America. In Midwestern United States, prevalence increased quickly in the first year of invasion (2012-13) but with low population declines. In the second year (2013-14), environmental contamination led to earlier infection and high population declines. Interventions must be implemented before or soon after fungal invasion to prevent population collapse.

Seasonal patterns in pathogen transmission can influence the impact of disease on populations and the speed of spatial spread. Increases in host contact rates or births drive seasonal epidemics in some systems, but other factors may occasionally override these influences. White-nose syndrome, caused by the emerging fungal pathogen Pseudogymnoascus destructans, is spreading across North America and threatens several bat species with extinction. We examined patterns and drivers of seasonal transmission of P. destructans by measuring infection prevalence and pathogen loads in six bat species at 30 sites across the eastern United States. Bats became transiently infected in autumn, and transmission spiked in early winter when bats began hibernating. Nearly all bats in six species became infected by late winter when infection intensity peaked. In summer, despite high contact rates and a birth pulse, most bats cleared infections and prevalence dropped to zero. These data suggest the dominant driver of seasonal transmission dynamics was a change in host physiology, specifically hibernation. Our study is the first, to the best of our knowledge, to describe the seasonality of transmission in this emerging wildlife disease. The timing of infection and fungal growth resulted in maximal population impacts, but only moderate rates of spatial spread.

White-Nose Syndrome (WNS) is an epizootic disease in hibernating bats caused by the fungus Pseudogymnoascus destructans. Surveillance for P. destructans at bat hibernacula consists primarily of visual surveys of bats, collection of potentially infected bats, and submission of these bats for laboratory testing. Cryptic infections (bats that are infected but display no visual signs of fungus) could lead to the mischaracterization of the infection status of a site and the inadvertent spread of P. destructans. We determined the efficacy of visual detection of P. destructans by examining visual signs and molecular detection of P. destructans on 928 bats of six species at 27 sites during surveys conducted from January through March in 2012-2014 in the southeastern USA on the leading edge of the disease invasion. Cryptic infections were widespread with 77% of bats that tested positive by qPCR showing no visible signs of infection. The probability of exhibiting visual signs of infection increased with sampling date and pathogen load, the latter of which was substantially higher in three species (Myotis lucifugus, M. septentrionalis, and Perimyotis subflavus). In addition, M. lucifugus was more likely to show visual signs of infection than other species given the same pathogen load. Nearly all infections were cryptic in three species (Eptesicus fuscus, M. grisescens, and M. sodalis), which had much lower fungal loads. The presence of M. lucifugus or M. septentrionalis at a site increased the probability that P. destructans was visually detected on bats. Our results suggest that cryptic infections of P. destructans are common in all bat species, and visible infections rarely occur in some species. However, due to very high infection prevalence and loads in some species, we estimate that visual surveys examining at least 17 individuals of M. lucifugus and M. septentrionalis, or 29 individuals of P. subflavus are still effective to determine whether a site has bats infected with P. destructans. In addition, because the probability of visually detecting the fungus was higher later in winter, surveys should be done as close to the end of the hibernation period as possible.

Brucella species include important zoonotic pathogens that have a substantial impact on both agriculture and human health throughout the world. Brucellae are thought of as "stealth pathogens" that escape recognition by the host innate immune response, modulate the acquired immune response, and evade intracellular destruction. We analyzed the genome sequences of members of the family Brucellaceae to assess its evolutionary history from likely free-living soil-based progenitors into highly successful intracellular pathogens. Phylogenetic analysis split the genus into two groups: recently identified and early-dividing "atypical" strains and a highly conserved "classical" core clade containing the major pathogenic species. Lateral gene transfer events brought unique genomic regions into Brucella that differentiated them from Ochrobactrum and allowed the stepwise acquisition of virulence factors that include a type IV secretion system, a perosamine-based O antigen, and systems for sequestering metal ions that are absent in progenitors. Subsequent radiation within the core Brucella resulted in lineages that appear to have evolved within their preferred mammalian hosts, restricting their virulence to become stealth pathogens capable of causing long-term chronic infections.