Title: Host traits and environment interact to drive host-pathogen coexistence following pathogen invasion
Running title: Mechanisms of host-pathogen coexistence
Manuscript format: Nature
Article type: Letter
Author line: Alexander T. Grimaudo1, Joseph R. Hoyt1, Steffany A. Yamada1, Carl J. Herzog2, Alyssa B. Bennett3, and Kate E. Langwig1
Affiliation: 1Department of Biological Sciences, Virginia Tech, Blacksburg, Virginia, 24060. 2New York State Department of Environmental Conservation, Albany, New York, 12233.3Vermont Fish and Wildlife Department, Montpelier, Vermont, 05602
Corresponding author: at.grimaudo@gmail.com, Steger Hall Room 363-3, 1015 Life Science Circle, Blacksburg, Virginia 24061
Statement of authorship: Conceptualization, ATG, JRH, and KEL; Methodology, ATG, JRH, and KEL; Formal Analysis, ATG and KEL; Investigation, ATG, JRH, SAY, CJH, ABB, and KEL; Data Curation, ATG, JRH, and KEL; Writing – Original Draft, ATG; Writing – Review & Editing, ATG, JRH, SAY, CJH, ABB, and KEL; Visualization, ATG; Supervision, JRH and KEL; and Project Administration, JRH and KEL.
Data accessibility statement: Should our manuscript be accepted, the data supporting the results will be archived in Dryad and the data DOI will be included at the end of the article
Keywords: temperature-mediated effects; host-pathogen coexistence; geographic mosaics; eco-evolutionary dynamics; emerging infectious disease; host resistance; host tolerance
Words in abstract: 188
Words in main text: 4,683
References: 123
Figures: 5
ABSTRACT
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 stabilization for reasons that are frequently unclear. While host, pathogen, and the environment are recognized 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 populations a decade after they declined 70-99% and subsequently stabilized with disease. 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.
INTRODUCTION
Emerging infectious diseases of wildlife have resulted in severe mortality events and regional to complete extinctions of host populations1–6. In some instances, the presence of pathogen reservoirs, frequency-dependent transmission, and small pre-epidemic host population sizes suggest that host species will be driven to extinction7. Additionally, high initial host population declines leave remnant populations more vulnerable to stochastic and Allee effects that increase the likelihood of host extinction7–9. However, following the initial epidemic and population declines, some host populations stabilize and persist for unknown reasons3,10,11. For example, population persistence has been observed in several important disease systems including amphibians impacted by chytridiomycosis10–14, Tasmanian devils impacted by facial tumor disease15–18, birds impacted by avian malaria19, and bats impacted by white-nose syndrome3,20. While initial evidence suggested that these host populations would be extirpated by infectious disease, some populations have stabilized despite infection prevalence remaining high while others continue to decline or have gone extinct3,5,26,10,11,16,21–25.
Potential drivers of host-pathogen coexistence include the evolution of host resistance, tolerance, and/or general vigor27–35, environmental refugia from infection or severe disease36–41, host demographic compensation13,42–45, density-dependent transmission46–49, and attenuation of pathogen virulence50–55. However, studies investigating host coexistence with virulent pathogens frequently focus on a single aspect of the host-pathogen-environment interaction, which may provide incomplete information on how host populations actually persist with disease. Given that many mechanisms of host population persistence include interactions between hosts and the environment, which may change as pathogen invasion progresses, understanding these interactions is essential for identifying the conditions necessary for host-pathogen coexistence following the invasion of a virulent pathogen.
White-nose syndrome (WNS) is an infectious disease of bats caused by the fungal pathogen Pseudogymnoascus destructans 56–58. In North America, the disease was first detected in New York state in 200659 and has since resulted in large mortality events and regional extinctions of once common bat species3,21,24. Bats become infected with P. destructans upon entering hibernacula in the fall60, and both indirect and direct transmission result in widespread infection early in the seasonal epidemic22,56,60,61. An environmental pathogen reservoir is established following the introduction of the pathogen to a hibernaculum22,62 and most populations decline greater than 90%, often resulting in complete local extirpations3,63. However, bats that survive hibernation emerge onto the landscape in spring and clear infection60,64,65.
The growth of P. destructans is sensitive to environmental temperature66 and humidity67, resulting in environmental trends in population declines such that populations and species roosting in warmer and wetter environments have more severe declines3,24,68–70. However, several years following pathogen introduction, some colonies of little brown bats (Myotis lucifugus ) in the northeast United States stabilized at 5-30% of their pre-epidemic population size following cumulative regional declines of 96%3,21,23,71,72 despite infection prevalence remaining high72. The isolate ofP. destructans collected from bats following its introduction to North America reproduces asexually73,74, and genetic evidence indicates the pathogen has changed little since the initial introduction73,75, suggesting virulence attenuation is not likely the principal driver of host-pathogen coexistence in this system. Additionally, the abiotic pathogen reservoir within hibernacula sustains a high prevalence of infection regardless of colony size, suggesting density-dependent transmission is also not a driver of population persistence22,60,76,77. Compared to colonies undergoing epidemic conditions on the invasion front, bats in persisting colonies display slower on-host pathogen growth rates, potentially a signature of host resistance72. However, persisting colonies also utilize colder hibernacula3,69, so lower pathogen growth rates may be a product of temperature operating independently of host characteristics.
The relative role of host traits and environmental conditions in driving the persistence of little brown bat populations impacted by WNS is still unclear. Understanding the factors driving host persistence will provide empirical support for general theory on host coexistence with virulent pathogens and much needed information on this important and devastating wildlife disease. Ten years following the introduction of P. destructans and subsequent colony declines, we conducted a fully factorial translocation experiment to understand the mechanisms of population persistence. We leveraged the variable environmental conditions in hibernacula (Fig. 1, Supplemental Fig. 1, 2) and a previously conducted translocation experiment early in the epizootic to disentangle the relative roles of host traits and environmental conditions in driving disease severity and ultimately population persistence.
RESULTS