Publisher Correction: Cryptic connections illuminate pathogen transmission within community networks.

In Fig. 3d this Letter, the R2 value should have been '0.19' instead of '0.66'; this has been corrected online.

Cryptic connections illuminate pathogen transmission within community networks.

Understanding host interactions that lead to pathogen transmission is fundamental to the prediction and control of epidemics1-5. Although the majority of transmissions often occurs within social groups6-9, the contribution of connections that bridge groups and species to pathogen dynamics is poorly understood10-12. 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 populations13-15. 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.

Sex-biased infections scale to population impacts for an emerging wildlife disease.

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.

Shifting effects of host physiological condition following pathogen establishment.

Understanding host persistence with emerging pathogens is essential for conserving populations. Hosts may initially survive pathogen invasions through pre-adaptive mechanisms. However, whether pre-adaptive traits are directionally selected to increase in frequency depends on the heritability and environmental dependence of the trait and the costs of trait maintenance. Body condition is likely an important pre-adaptive mechanism aiding in host survival, although can be seasonally variable in wildlife hosts. We used data collected over 7 years on bat body mass, infection and survival to determine the role of host body condition during the invasion and establishment of the emerging disease, white-nose syndrome. We found that when the pathogen first invaded, bats with higher body mass were more likely to survive, but this effect dissipated following the initial epizootic. We also found that heavier bats lost more weight overwinter, but fat loss depended on infection severity. Lastly, we found mixed support that bat mass increased in the population after pathogen arrival; high annual plasticity in individual bat masses may have reduced the potential for directional selection. Overall, our results suggest that some factors that contribute to host survival during pathogen invasion may diminish over time and are potentially replaced by other host adaptations.

Environmental reservoir dynamics predict global infection patterns and population impacts for the fungal disease white-nose syndrome.

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.

Host traits and environment interact to determine persistence of bat populations impacted by white-nose syndrome.

Emerging infectious diseases have resulted in severe population declines across diverse taxa. In some instances, despite attributes associated with high extinction risk, disease emergence and host declines are followed by host stabilisation for unknown reasons. While host, pathogen, and the environment are recognised as important factors that interact to determine host-pathogen coexistence, they are often considered independently. Here, we use a translocation experiment to disentangle the role of host traits and environmental conditions in driving the persistence of remnant bat populations a decade after they declined 70-99% due to white-nose syndrome and subsequently stabilised. While survival was significantly higher than during the initial epidemic within all sites, protection from severe disease only existed within a narrow environmental space, suggesting host traits conducive to surviving disease are highly environmentally dependent. Ultimately, population persistence following pathogen invasion is the product of host-pathogen interactions that vary across a patchwork of environments.

Mobility and infectiousness in the spatial spread of an emerging fungal pathogen.

Emerging infectious diseases can have devastating effects on host communities, causing population collapse and species extinctions. The timing of novel pathogen arrival into naïve species communities can have consequential effects that shape the trajectory of epidemics through populations. Pathogen introductions are often presumed to occur when hosts are highly mobile. However, spread patterns can be influenced by a multitude of other factors including host body condition and infectiousness. White-nose syndrome (WNS) is a seasonal emerging infectious disease of bats, which is caused by the fungal pathogen Pseudogymnoascus destructans. Within-site transmission of P. destructans primarily occurs over winter; however, the influence of bat mobility and infectiousness on the seasonal timing of pathogen spread to new populations is unknown. We combined data on host population dynamics and pathogen transmission from 22 bat communities to investigate the timing of pathogen arrival and the consequences of varying pathogen arrival times on disease impacts. We found that midwinter arrival of the fungus predominated spread patterns, suggesting that bats were most likely to spread P. destructans when they are highly infectious, but have reduced mobility. In communities where P. destructans was detected in early winter, one species suffered higher fungal burdens and experienced more severe declines than at sites where the pathogen was detected later in the winter, suggesting that the timing of pathogen introduction had consequential effects for some bat communities. We also found evidence of source-sink population dynamics over winter, suggesting some movement among sites occurs during hibernation, even though bats at northern latitudes were thought to be fairly immobile during this period. Winter emergence behaviour symptomatic of white-nose syndrome may further exacerbate these winter bat movements to uninfected areas. Our results suggest that low infectiousness during host migration may have reduced the rate of expansion of this deadly pathogen, and that elevated infectiousness during winter plays a key role in seasonal transmission. Furthermore, our results highlight the importance of both accurate estimation of the timing of pathogen spread and the consequences of varying arrival times to prevent and mitigate the effects of infectious diseases.

Pathogen dynamics during invasion and establishment of white-nose syndrome explain mechanisms of host persistence.

Disease dynamics during pathogen invasion and establishment determine the impacts of disease on host populations and determine the mechanisms of host persistence. Temporal progression of prevalence and infection intensity illustrate whether tolerance, resistance, reduced transmission, or demographic compensation allow initially declining populations to persist. We measured infection dynamics of the fungal pathogen Pseudogymnoascus destructans that causes white-nose syndrome in bats by estimating pathogen prevalence and load in seven bat species at 167 hibernacula over a decade as the pathogen invaded, became established, and some host populations stabilized. Fungal loads increased rapidly and prevalence rose to nearly 100% at most sites within 2 yr of invasion in six of seven species. Prevalence and loads did not decline over time despite huge reductions in colony sizes, likely due to an extensive environmental reservoir. However, there was substantial variation in fungal load among sites with persisting colonies, suggesting that both tolerance and resistance developed at different sites in the same species. In contrast, one species disappeared from hibernacula within 3 yr of pathogen invasion. Variable host responses to pathogen invasion require different management strategies to prevent disease-induced extinction and to facilitate evolution of tolerance or resistance in persisting populations.

Host persistence or extinction from emerging infectious disease: insights from white-nose syndrome in endemic and invading regions.

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.

Invasion dynamics of white-nose syndrome fungus, midwestern United States, 2012-2014.

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.

Host and pathogen ecology drive the seasonal dynamics of a fungal disease, white-nose syndrome.

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.

Interannual Survival of Myotis lucifugus (Chiroptera: Vespertilionidae) near the Epicenter of White-Nose Syndrome.

Reduced populations of Myotis lucifugus (Little Brown Myotis) devastated by white-nose syndrome (WNS) persist in eastern North America. Between 2009 and 2013, we recaptured 113 marked individuals that survived between 1 and 6 winters in New England since the arrival of WNS. We also observed signs of reproductive success in 57 recaptured bats.

Prior exposure to pathogens augments host heterogeneity in susceptibility and has key epidemiological consequences.

Pathogen epidemics are key threats to human and wildlife health. Across systems, host protection from pathogens following initial exposure is often incomplete, resulting in recurrent epidemics through partially-immune hosts. Variation in population-level protection has important consequences for epidemic dynamics, but whether acquired protection influences host heterogeneity in susceptibility and its epidemiological consequences remains unexplored. We experimentally investigated whether prior exposure (none, low-dose, or high-dose) to a bacterial pathogen alters host heterogeneity in susceptibility among songbirds. Hosts with no prior pathogen exposure had little variation in protection, but heterogeneity in susceptibility was significantly augmented by prior pathogen exposure, with the highest variability detected in hosts given high-dose prior exposure. An epidemiological model parameterized with experimental data found that heterogeneity in susceptibility from prior exposure more than halved epidemic sizes compared with a homogeneous population with identical mean protection. However, because infection-induced mortality was also greatly reduced in hosts with prior pathogen exposure, reductions in epidemic size were smaller than expected in hosts with prior exposure. These results highlight the importance of variable protection from prior exposure and/or vaccination in driving host heterogeneity and epidemiological dynamics.

Host infection and disease-induced mortality modify species contributions to the environmental reservoir.

Environmental pathogen reservoirs exist for many globally important diseases and can fuel epidemics, influence pathogen evolution, and increase the threat of host extinction. Species composition can be an important factor that shapes reservoir dynamics and ultimately determines the outcome of a disease outbreak. However, disease-induced mortality can change species communities, indicating that species responsible for environmental reservoir maintenance may change over time. Here we examine the reservoir dynamics of Pseudogymnoascus destructans, the fungal pathogen that causes white-nose syndrome in bats. We quantified changes in pathogen shedding, infection prevalence and intensity, host abundance, and the subsequent propagule pressure imposed by each species over time. We find that highly shedding species are important during pathogen invasion, but contribute less over time to environmental contamination as they also suffer the greatest declines. Less infected species remain more abundant, resulting in equivalent or higher propagule pressure. More broadly, we demonstrate that high infection intensity and subsequent mortality during disease progression can reduce the contributions of high-shedding species to long-term pathogen maintenance.

White-nose syndrome restructures bat skin microbiomes.

IMPORTANCE: Inherent 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.

Environmental transmission of Pseudogymnoascus destructans to hibernating little brown bats.

Pathogens with persistent environmental stages can have devastating effects on wildlife communities. White-nose syndrome (WNS), caused by the fungus Pseudogymnoascus destructans, has caused widespread declines in bat populations of North America. In 2009, during the early stages of the WNS investigation and before molecular techniques had been developed to readily detect P. destructans in environmental samples, we initiated this study to assess whether P. destructans can persist in the hibernaculum environment in the absence of its conclusive bat host and cause infections in naive bats. We transferred little brown bats (Myotis lucifugus) from an unaffected winter colony in northwest Wisconsin to two P. destructans contaminated hibernacula in Vermont where native bats had been excluded. Infection with P. destructans was apparent on some bats within 8 weeks following the introduction of unexposed bats to these environments, and mortality from WNS was confirmed by histopathology at both sites 14 weeks following introduction. These results indicate that environmental exposure to P. destructans is sufficient to cause the infection and mortality associated with WNS in naive bats, which increases the probability of winter colony extirpation and complicates conservation efforts.

Sociality, density-dependence and microclimates determine the persistence of populations suffering from a novel fungal disease, white-nose syndrome.

Disease has caused striking declines in wildlife and threatens numerous species with extinction. Theory suggests that the ecology and density-dependence of transmission dynamics can determine the probability of disease-caused extinction, but few empirical studies have simultaneously examined multiple factors influencing disease impact. We show, in hibernating bats infected with Geomyces destructans, that impacts of disease on solitary species were lower in smaller populations, whereas in socially gregarious species declines were equally severe in populations spanning four orders of magnitude. However, as these gregarious species declined, we observed decreases in social group size that reduced the likelihood of extinction. In addition, disease impacts in these species increased with humidity and temperature such that the coldest and driest roosts provided initial refuge from disease. These results expand our theoretical framework and provide an empirical basis for determining which host species are likely to be driven extinct while management action is still possible.

Risk factors associated with mortality from white-nose syndrome among hibernating bat colonies.

White-nose syndrome (WNS) is a disease responsible for unprecedented mortality in hibernating bats. First observed in a New York cave in 2006, mortality associated with WNS rapidly appeared in hibernacula across the northeastern United States. We used yearly presence-absence data on WNS-related mortality among hibernating bat colonies in the Northeast to determine factors influencing its spread. We evaluated hazard models to test hypotheses about the association between the timing of mortality and colony-level covariates, such as distance from the first WNS-affected site, colony size, species diversity, species composition and type of hibernaculum (cave or mine). Distance to origin and colony size had the greatest effects on WNS hazard over the range of observations; the type of hibernaculum and species composition had weaker effects. The distance effect showed a temporal decrease in magnitude, consistent with the pattern of an expanding epizootic. Large, cave-dwelling bat colonies with high proportions of Myotis lucifugus or other species that seek humid microclimates tended to experience early mortality. Our results suggest that the timing of mortality from WNS is largely dependent on colony location, and large colonies tend to be first in an area to experience high mortality associated with WNS.

Ecology and impacts of white-nose syndrome on bats.

The recent introduction of Pseudogymnoascus destructans (the fungal pathogen that causes white-nose syndrome in bats) from Eurasia to North America has resulted in the collapse of North American bat populations and restructured species communities. The long evolutionary history between P. destructans and bats in Eurasia makes understanding host life history essential to uncovering the ecology of P. destructans. In this Review, we combine information on pathogen and host biology to understand the patterns of P. destructans spread, seasonal transmission ecology, the pathogenesis of white-nose syndrome and the cross-scale impact from individual hosts to ecosystems. Collectively, this research highlights how early pathogen detection and quantification of host impacts has accelerated the understanding of this newly emerging infectious disease.