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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.

Disease can play an important role in structuring species communities because the effects of disease vary among hosts; some species are driven towards extinction, while others suffer relatively little impact. Why disease impacts vary among host species remains poorly understood for most multi-host pathogens, and factors allowing less-susceptible species to persist could be useful in conserving highly affected species. White-nose syndrome (WNS), an emerging fungal disease of bats, has decimated some species while sympatric and closely related species have experienced little effect. We analysed data on infection prevalence, fungal loads and environmental factors to determine how variation in infection among sympatric host species influenced the severity of WNS population impacts. Intense transmission resulted in almost uniformly high prevalence in all species. By contrast, fungal loads varied over 3 orders of magnitude among species, and explained 98% of the variation among species in disease impacts. Fungal loads increased with hibernating roosting temperatures, with bats roosting at warmer temperatures having higher fungal loads and suffering greater WNS impacts. We also found evidence of a threshold fungal load, above which the probability of mortality may increase sharply, and this threshold was similar for multiple species. This study demonstrates how differences in behavioural traits among species—in this case microclimate preferences—that may have been previously adaptive can be deleterious after the introduction of a new pathogen. Management to reduce pathogen loads rather than exposure may be an effective way of reducing disease impact and preventing species extinctions. This article is part of the themed issue ‘Tackling emerging fungal threats to animal health, food security and ecosystem resilience’.

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.

Yersinia pestis, the etiologic agent of the disease plague, has been implicated in three historical pandemics. These include the third pandemic of the 19(th) and 20(th) centuries, during which plague was spread around the world, and the second pandemic of the 14(th)-17(th) centuries, which included the infamous epidemic known as the Black Death. Previous studies have confirmed that Y. pestis caused these two more recent pandemics. However, a highly spirited debate still continues as to whether Y. pestis caused the so-called Justinianic Plague of the 6(th)-8(th) centuries AD. By analyzing ancient DNA in two independent ancient DNA laboratories, we confirmed unambiguously the presence of Y. pestis DNA in human skeletal remains from an Early Medieval cemetery. In addition, we narrowed the phylogenetic position of the responsible strain down to major branch 0 on the Y. pestis phylogeny, specifically between nodes N03 and N05. Our findings confirm that Y. pestis was responsible for the Justinianic Plague, which should end the controversy regarding the etiology of this pandemic. The first genotype of a Y. pestis strain that caused the Late Antique plague provides important information about the history of the plague bacillus and suggests that the first pandemic also originated in Asia, similar to the other two plague pandemics.

Pathogens that persist in an environmental reservoir can drive host populations to extinction because host abundance does not limit pathogen survival or reproduction. Fungal pathogens are of particular conservation concern because many fungi are generalists that persist in the environment. One example is Pseudogymnoascus destructans , the causative agent of white-nose syndrome (WNS), which has caused severe declines in hibernating bat populations across North America. Treatment of environmental reservoirs could help reduce transmission of P. destructans , and thus, reduce bat population declines from WNS. We tested the efficacy of two environmental cleaning agents, ultraviolet-C radiation and polyethylene glycol, in three mines where P. destructans established an environmental reservoir and caused declines in winter colony size of hibernating bats in Ontario, Alabama, and Arkansas. We observed considerable variation between sites but, based on our experimental design, treatments did not reduce environmental P. destructans prevalence or load and there was no consistent pattern in response to the treatments across mines. More encouragingly, treatments did not impact non-target fungi or bacteria. Our results could reflect aspects of our experimental design, including relatively small treatment cells and the lack of an available assay to assess viability of P. destructans from swab samples. Among-site variation we observed, combined with positive results of these treatments in other studies, suggest that site-specific management responses may be important for reducing impacts of white-nose syndrome on bat populations.

Insectivorous bats consume a diverse array of arthropod prey, with diets varying by bat species, sampling location, and season. North American bat diets remain incompletely described, which is concerning at a time when many bat and insect populations appear to be declining. Understanding the variability in foraging is thus an essential component for effective bat conservation. To comprehensively evaluate local foraging, we assessed the spatial and temporal variability in prey consumed by the little brown bat, Myotis lucifugus , in New Hampshire, USA. We collected bat guano samples from 20 sites over 2 years and analyzed sequence data for 899 of these samples using a molecular metabarcoding approach targeting the cytochrome oxidase I subunit (COI) gene. Some prey items were broadly shared across locations and sampling dates, with the most frequently detected arthropod orders broadly similar to previous morphological and molecular analyses; at least one representative sequence variant was assigned to Coleoptera in 92% of samples, with other frequently detected orders including Diptera (73%), Lepidoptera (65%), Trichoptera (38%), and Ephemeroptera (32%). More specifically, two turf and forest pests were routinely detected: white grubs in the genus Phyllophaga (50%), and the Asiatic Garden beetle, Maladera castanea (36%). Despite the prevalence of a few taxa shared among many samples and distinct seasonal peaks in consumption of specific arthropods, diet composition varied both temporally and spatially. However, species richness did not strongly vary indicating consumption of a broad diversity of taxa throughout the summer. These data characterize little brown bats as flexible foragers adept at consuming a broad array of locally available prey resources.

Understanding host interactions that lead to pathogen transmission is fundamental to the prediction and control of epidemics 1 – 5 . Although the majority of transmissions often occurs within social groups 6 – 9 , the contribution of connections that bridge groups and species to pathogen dynamics is poorly understood 10 – 12 . These cryptic connections—which are often indirect or infrequent—provide transmission routes between otherwise disconnected individuals and may have a key role in large-scale outbreaks that span multiple populations or species. Here we quantify the importance of cryptic connections in disease dynamics by simultaneously characterizing social networks and tracing transmission dynamics of surrogate-pathogen epidemics through eight communities of bats. We then compared these data to the invasion of the fungal pathogen that causes white-nose syndrome, a recently emerged disease that is devastating North American bat populations 13 – 15 . We found that cryptic connections increased links between individuals and between species by an order of magnitude. Individuals were connected, on average, to less than two per cent of the population through direct contact and to only six per cent through shared groups. However, tracing surrogate-pathogen dynamics showed that each individual was connected to nearly fifteen per cent of the population, and revealed widespread transmission between solitarily roosting individuals as well as extensive contacts among species. Connections estimated from surrogate-pathogen epidemics, which include cryptic connections, explained three times as much variation in the transmission of the fungus that causes white-nose syndrome as did connections based on shared groups. These findings show how cryptic connections facilitate the community-wide spread of pathogens and can lead to explosive epidemics. Cryptic connections facilitate the community-wide spread of disease both within and among species.

Two aspects of host infectiousness shape pathogen transmission and distribution but are underappreciated: the relationship between pathogen load and infectiousness, and variability in pathogen load within species. We quantified the relationship between host pathogen load (parasitemia) for avian malaria ( Plasmodium relictum ) and infectiousness for biting Culex quinquefasciatus mosquitoes with experimental infections in canaries ( Serinus canaria ). Using this relationship, we estimated the infectiousness of 17 bird species in 11 communities in Hawaiʻi and quantified the relative contributions of infection stage (acute versus chronic) to transmission. We show that infectiousness to mosquitoes increased with parasitemia, temperature, and time since feeding. The relationship’s gradual (low) parasitemia slope resulted in a wide range of parasitemias being partly infectious, and high within-host species variability in parasitemia led to extensive overlap in infectiousness among hosts. Disproportionate mosquito host utilization (inferred from relative infection prevalence) elevated the importance of a few host species, yet broad overlap in species infectiousness resulted in similar total infectiousness across most bird communities. This similarity likely contributed to avian malaria’s widespread distribution throughout Hawaiʻi despite diverse host community assemblages. Our findings highlight the importance of both the shape of the pathogen load–infectiousness relationship and within-species variability in determining a pathogen’s host range, transmission intensity, and spatial spread. The combination of within-species variation in pathogen load, the shape of the relationship between pathogen load and infectiousness, and vector feeding preferences shape transmission of multi-host vector-borne pathogens. Here, the authors use experimental and wild bird infection data to characterize the role of 17 host bird species in avian malaria transmission in Hawaii.

Globalization has facilitated the worldwide movement and introduction of pathogens, but epizoological reconstructions of these invasions are often hindered by limited sampling and insufficient genetic resolution among isolates. Pseudogymnoascus destructans , a fungal pathogen causing the epizootic of white-nose syndrome in North American bats, has exhibited few genetic polymorphisms in previous studies, presenting challenges for both epizoological tracking of the spread of this fungus and for determining its evolutionary history. We used single nucleotide polymorphisms (SNPs) from whole-genome sequencing and microsatellites to construct high-resolution phylogenies of P. destructans . Shallow genetic diversity and the lack of geographic structuring among North American isolates support a recent introduction followed by expansion via clonal reproduction across the epizootic zone. Moreover, the genetic relationships of isolates within North America suggest widespread mixing and long-distance movement of the fungus. Genetic diversity among isolates of P. destructans from Europe was substantially higher than in those from North America. However, genetic distance between the North American isolates and any given European isolate was similar to the distance between the individual European isolates. In contrast, the isolates we examined from Asia were highly divergent from both European and North American isolates. Although the definitive source for introduction of the North American population has not been conclusively identified, our data support the origin of the North American invasion by P. destructans from Europe rather than Asia. IMPORTANCE This phylogenetic study of the bat white-nose syndrome agent, P. destructans , uses genomics to elucidate evolutionary relationships among populations of the fungal pathogen to understand the epizoology of this biological invasion. We analyze hypervariable and abundant genetic characters (microsatellites and genomic SNPs, respectively) to reveal previously uncharacterized diversity among populations of the pathogen from North America and Eurasia. We present new evidence supporting recent introduction of the fungus to North America from a diverse Eurasian population, with limited increase in genetic variation in North America since that introduction. This phylogenetic study of the bat white-nose syndrome agent, P. destructans , uses genomics to elucidate evolutionary relationships among populations of the fungal pathogen to understand the epizoology of this biological invasion. We analyze hypervariable and abundant genetic characters (microsatellites and genomic SNPs, respectively) to reveal previously uncharacterized diversity among populations of the pathogen from North America and Eurasia. We present new evidence supporting recent introduction of the fungus to North America from a diverse Eurasian population, with limited increase in genetic variation in North America since that introduction.

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.