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