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Langwig, K. E.

Publications and source records attributed to Langwig, K. E..

16 recordsLinked to original sources

Amplified transmission in host communities following disease-induced declines

Pathogen transmission is a fundamental component of infectious disease systems, governing the speed and extent of pathogen outbreaks. Predicting transmission within and among species is therefore critical for outbreak preparedness and the effective implementation of control strategies. Epidemics themselves can alter host populations in ways that fundamentally reshape transmission, but the long-term consequences remain poorly understood. Here, we quantify changes in transmission using a surrogate pathogen in bat communities before and after the emergence of white-nose syndrome, a fungal disease that has caused widespread population declines across North America. We find that transmission increased following disease-induced declines across all species in the community. We also observed an increase in environmental contacts and expanded habitat use by individuals, suggesting that surviving bats, on average, increased their activity and opportunities for interaction despite the substantial reductions in density and costs of infection. Together, these findings demonstrate that pathogen emergence can fundamentally alter host contact patterns and transmission dynamics, emphasizing the importance of considering behavioral and ecological changes imposed by epidemics when predicting pathogen spread in naive host populations.

ecology↗

Environmental conditions drive selection and recovery following disease-induced declines

Emerging infectious diseases threaten public health and biodiversity across the globe1,2. Disease outcomes are frequently dependent on local environmental conditions3-5, but how these factors shape host adaptation and long-term recovery are often unknown6. Here we combine two decades of population, disease, and environmental data with a common garden experiment to investigate the drivers of variable declines and recovery for remnant bat populations following the emergence of the fungal disease, white-nose syndrome. We find that initial declines were greater and faster in warmer sites (88.3% vs. 74.2% in cold sites), but these populations recovered more quickly and hosts developed higher resistance (1.5x reduction of fungal loads) than populations from colder sites that were buffered from initial impacts. Our experimental data suggest that warm sites served as hotspots of host adaptation where selective pressures were stronger because thermal conditions approached optimal growth for the pathogen, which eventually favored the development of high pathogen resistance. Populations in colder sites experienced weaker selective pressure and thus remain more susceptible, although bats from larger colonies were more likely to survive, suggesting that adaptive traits exist in these populations, but at much lower frequency. These findings show that the environmental conditions that initially buffer populations from collapse can simultaneously constrain their evolutionary response to emerging threats, and ultimately determine differential recovery following disease-induced declines.

ecology↗

Paying upfront: successful initial infections protect against severe future infections

Understanding the consistency with which individual hosts respond to repeated pathogen exposures is crucial for accurately modeling pathogen transmission and eco-evolutionary dynamics. When hosts face repeated pathogen exposures, immune memory is expected to reduce the probability and/or severity of subsequent infections, yet it remains unclear whether individuals remain consistent in their level of response relative to others. We investigated this question in house finches (Haemorhous mexicanus) from two populations varying in history of endemism of the bacterial pathogen Mycoplasma gallisepticum (MG). Individuals were confirmed to be MG-naive at capture and then experimentally inoculated twice with MG, allowing recovery between inoculations. We then asked if host responses to the second inoculation were predicted by responses to initial inoculation, sex, or population of origin. Our results suggest that individuals were not consistent in their relative response levels; rather, a successful initial infection provided protection against a severe second infection, increasing both tolerance and resistance. While we found no population differences in response to the second inoculation, males showed higher susceptibility to the second inoculation than females. Investigating and accounting for individual variation in response to subsequent exposures may improve the precision and accuracy of transmission models for wildlife pathogens.

ecology↗

Host prior exposure augments heterogeneity in gene expression in both host and pathogen during in vivo infection

Variability in acquired protection, whether from prior pathogen exposure or vaccination, is increasingly recognized as a key determinant of host population-level variation in disease traits. It remains unclear whether this extends to the within-host physiological environment and what the consequences are for reinfecting pathogens. Here, we asked whether prior pathogen exposure of hosts induces gene expression heterogeneity in the host and/or pathogen during infection. We quantified gene expression in vivo following high-dose pathogen challenge of house finches (Haemorhous mexicanus) previously given controlled, varied exposure histories to a bacterial pathogen (Mycoplasma gallisepticum; MG). To measure gene expression heterogeneity, we collected transcriptomic data from two host tissues (conjunctiva and spleen), and, simultaneously, from pathogen infecting the primary site of infection (conjunctiva). In the conjunctiva, but not the spleen, prior pathogen exposure induced significant heterogeneity in host gene expression relative to pathogen-naive hosts. Further, hosts that received a lower prior exposure dose rather than a higher primary dose showed the greatest within-group heterogeneity in expression during re-challenge. Functional enrichment analyses for significantly variable host genes indicated an over-representation of terms involved in the immune systems response to pathogens, namely a diversified inflammatory response, in birds with prior pathogen exposure. The infecting pathogen from the conjunctiva followed similar patterns of heterogeneity in host gene expression, where pathogen infecting hosts with prior exposure had more heterogeneous expression than those infecting pathogen-naive hosts. While the exact mechanisms that underlie greater variation in gene expression cannot be resolved by this study, our results are consistent with the hypothesis that prior host exposure induces a within-host environment that promotes heterogeneous gene expression across both hosts and pathogens. This suggests that to understand the coevolutionary dynamics of infectious diseases we must consider not only the genetic sequence variation, but also gene expression variation in host and pathogen.

ecology↗

Mating strategies explain sex-biased infections in an emerging fungal disease

O_LIMating dynamics can govern species impacts from rapid global change by influencing population rates of growth and adaptation, as well as individual traits that affect mortality risks from novel pressures. C_LIO_LIHere, we examined sex differences in activity of Myotis lucifugus during their mating season, which coincides with exposure to the lethal fungal pathogen (Pseudogymnoascus destructans) that causes white-nose syndrome. We expected differences in activity between sexes to modify seasonal P. destructans dynamics as the pathogen can replicate only at the cool temperatures at which bats hibernate. C_LIO_LIWe used passive antenna systems installed at the entrances of hibernacula and PIT tags to characterize activity patterns of bats. We also measured pathogen loads on bats during the autumn mating and early hibernation periods to assess how infection changed according to host phenology. C_LIO_LIWe found that females spent fewer days active during autumn, arrived after males, and were primarily active on the warmest nights. Males remained highly active throughout the mating season and later in autumn than females. Importantly, differences in phenology corresponded to higher pathogen loads on females during early hibernation as male activity, and thus warm body temperatures, inhibit pathogen growth. C_LIO_LIDifferences in activity between sexes and in the transition from swarm to hibernation likely reflects males maximizing their mating opportunities while females conserve energy to meet the cost of spring migration and reproduction. More broadly, our results show how activity during the mating season and phenology can contribute to sex-biased impacts of a novel disease and highlight the value of understanding species mating systems to anticipate the impacts of environmental change. C_LI

ecology↗

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 how acquired protection influences inter{-}individual heterogeneity in susceptibility and its epidemiological consequences remains understudied. 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 population-level heterogeneity and epidemiological dynamics.

microbiology↗

Drivers of population dynamics of at-risk populations change with pathogen arrival

Successful wildlife conservation in an era of rapid global change requires understanding determinants of species population abundance and growth. However, when populations are faced with novel stressors, factors associated with healthy and growing populations can change, necessitating a shift in conservation strategies. For example, emerging infectious diseases can cause conditions previously beneficial or neutral to host populations to increase disease impacts. Here, we paired a population dataset of 265 colonies of the federally endangered Indiana bat (Myotis sodalis) with 50.7 logger-years of environmental data to explore factors that affected colony response to white-nose syndrome (WNS), an emerging fungal disease. We found wide variation in colony responses to WNS, ranging from extirpation to stabilization and persistence. Simulating future population dynamics suggests that most extirpations have already occurred, as the pathogen has been present for several years in most colonies, and that small colonies were more susceptible to extirpation than large ones. Further, while temperature and humidity conditions of hibernacula appeared unassociated with Indiana bat colony growth prior to WNS, extirpation risk following pathogen arrival was elevated in colonies that used colder and wetter hibernacula. Additionally, rates of decline were greater in colder hibernacula, opposite the association for a sympatric bat species. Overall, this study illustrates that emerging infectious diseases can change the factors associated with host population abundance and optimal growth, including through novel environmental associations, which can vary across host species. Consideration of these shifting associations and intrinsic differences between impacted host species will be essential to successful species conservation.

ecology↗

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 seven 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 budgeting depended on infection severity. Lastly, we found little support that bat mass increased in the population after pathogen arrival, and there was high annual plasticity in individual bat masses. Overall, our results suggest that factors that contribute to host survival during pathogen invasion may diminish over time, and are potentially replaced by other host adaptations.

ecology↗

Wildlife exposure to SARS-CoV-2 across a human use gradient

Pervasive SARS-CoV-2 infections in humans have led to multiple transmission events to captive animals. While SARS-CoV-2 has a potential broad wildlife host range, most documented infections to date are found in a single species, the white-tailed deer. The extent of SARS-CoV-2 exposure among wildlife species and the factors that influence wildlife transmission risk remain unknown. We sampled 23 wildlife species for SARS-CoV-2 and examined the effects of urbanization and human use on seropositivity. Here, we document positive detections of SARS-CoV-2 RNA in six species, including the deer mouse, Virginia opossum, raccoon, groundhog, Eastern cottontail, and Eastern red bat. In addition, we found that sites with high human activity had three times higher seroprevalence than low human-use areas. We detected SARS-CoV-2 genomic sequences from nine individuals of six species which were assigned to seven Pango lineages of the Omicron variant. The close match to variants circulating in humans at the time suggests at least seven recent human-to-animal transmission events. Our data support that exposure to SARS-CoV-2 has been widespread in wildlife communities and suggests that areas with high human activity may serve as points of contact for cross-species transmission.

ecology↗

Host abundance and heterogeneity in infectiousness determine extent of 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 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.

ecology↗

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 behavior. 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.

ecology↗

Reducing environmentally mediated transmission to moderate impacts of an emerging wildlife disease

O_LIEmerging infectious diseases are a serious threat to wildlife communities, and the ability of pathogens to survive in the environment can exacerbate disease impacts on hosts and increase the likelihood of species extinction. Targeted removal or control of these environmental reservoirs could provide an effective mitigation strategy for reducing disease impacts but is rarely used in wildlife disease control. C_LIO_LIWe examined the effectiveness of managing environmental transmission to reduce impacts of an emerging infectious disease of bats, white-nose syndrome. We used a chemical disinfectant, chlorine dioxide (ClO2), to experimentally reduce Pseudogymnoascus destructans, the fungal pathogen causing WNS, in the environment. We conducted laboratory experiments followed by three years of field trials at four abandoned mines to determine whether ClO2 could effectively reduce P. destructans in the environment, reduce host infection, and limit population impacts. C_LIO_LIClO2 was effective at killing P. destructans in vitro across a range of concentrations. In field settings, higher concentrations of ClO2 treatment sufficiently reduced viable P. destructans conidia in the environment. C_LIO_LIThe reduction in the environmental reservoir at treatment sites resulted in lower fungal loads on bats compared to untreated control populations. Survival following treatment was higher in little brown bats (Myotis lucifugus), and trended higher for tricolored bats (Perimyotis subflavus) compared to untreated sites. C_LIO_LIThese findings support the management of environmental reservoirs as an effective control strategy for wildlife disease and provide a valuable tool for ongoing conservation efforts. More broadly, these results highlight how the intensity of environmental reservoirs can have cascading impacts on host infection and population declines. C_LI

ecology↗

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.

ecology↗

Tradeoffs between mobility and infectiousness in the spatial spread of an emerging pathogen

O_LIEmerging infectious diseases can have devastating effects on host communities, causing population collapse and species extinctions. The timing of novel pathogen arrival into naive 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. C_LIO_LIWhite-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. C_LIO_LIWe 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 behavior symptomatic of white-nose syndrome may further exacerbate these winter bat movements to uninfected areas. C_LIO_LIOur 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. C_LI

ecology↗

White-nose syndrome restructures bat skin microbiomes

The skin microbiome is an essential line of host defense against pathogens, yet our understanding of microbial communities and how they change when hosts become infected is limited. We investigated skin microbial composition in three North American bat species (Myotis lucifugus, Eptesicus fuscus, and Perimyotis subflavus) that have been impacted by the infectious disease, white-nose syndrome, caused by an invasive fungal pathogen, Pseudogymnoascus destructans. We compared bacterial and fungal composition from 154 skin swab samples and 70 environmental samples using a targeted 16S rRNA and ITS amplicon approach. We found that for M. lucifugus, a species that experiences high mortality from white-nose syndrome, bacterial microbiome diversity was dramatically lower when P. destructans is present. Key bacterial families--including those potentially involved in pathogen defense--significantly differed in abundance in bats infected with P. destructans compared to uninfected bats. However, skin bacterial diversity was not lower in E. fuscus or P. subflavus when P. destructans was present, despite populations of the latter species declining sharply from white-nose syndrome. The fungal species present on bats substantially overlapped with the fungal taxa present in the environment at the site where the bat was sampled, but fungal community composition was unaffected by the presence of P. destructans for any of the three bat species. This species-specific alteration in bat skin bacterial microbiomes after pathogen invasion may suggest a mechanism for the severity of WNS in M. lucifugus, but not for other bat species impacted by white-nose syndrome.

microbiology↗

Field trial of a probiotic bacteria and a chemical, chitosan, to protect bats from white-nose syndrome

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 two treatments, a probiotic bacterium, Pseudomonas fluorescens, and a chemical, chitosan, to reduce impacts of WNS in two simultaneous experiments conducted with caged and free-flying Myotis lucifugus bats at a mine in Wisconsin, USA. In the free-flying 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 30 days. Apparent overwinter survival for free-flying chitosan-treated bats was 18.0%, which did not differ significantly from control bats. In the cage experiment, chitosan-treated bats had significantly higher survival until release on March 8 (53%) than control and P. fluorescens-treated bats (both 27%). However, these differences were likely due to within-cage disturbance and not reduced WNS impacts, because chitosan-treated bats actually had significantly higher UV-fluorescence (a measure of disease severity), and body mass, not infection intensity, predicted mortality. Further, few of the bats released from the cage experiment were detected emerging from the mine, indicating that the survival estimates at the time of release did not carryover to overwinter survival. These results suggest that treatment of bats may reduce WNS mortality, but additional measures are needed to prevent declines.

ecology↗