Discussion
Our results demonstrate that Bd strains are typically more successful at
infecting and replicating, and thus causing mortality, in local than
novel hosts, supporting local adaptation or the hypothesis that
pathogens are best adapted to take advantage of their local hosts
(Lively & Jokela 1996; Kaltz & Shykoff 1998; Lively & Dybdahl 2000;
Morran et al. 2011; Strauss et al. 2012; Lymbery et
al. 2014; Urban et al. 2020; Johnson et al. 2021).
However, the rise of catastrophic modern pandemics from pathogen
pollution has led to speculation that introduced pathogens are
especially devastating to naïve hosts (Carey et al. 1999;
Cunningham et al. 2003; Anderson et al. 2004; Mastitskyet al. 2010). While we did find substantial variation among
host-pathogen outcomes, there was no evidence that novel host-pathogen
interactions generally cause especially high mortality. Thus, the major
concern with pathogen pollution is not that naïve hosts are especially
vulnerable but that increasing introductions of novel pathogens
increases the chance that virulent pathogens will encounter highly
vulnerable hosts. This perception that novel and introduced pathogens
are especially deadly might be because of detection bias – most
introduced pathogens might go undetected because low pathogen fitness in
novel host populations reduces the likelihood of establishment (Torchinet al. 2003; Torchin & Mitchell 2004). However, there are
>8,000 species of amphibians and a multitude of Bd strains
and thus the full strength of local adaptation and the scope of
variation in host-strain outcomes remains unclear in this system.
We found significant variation in mortality, infection success, and
pathogen load among Bd strains (Figure 3 & S2), consistent with other
studies showing variation in the traits of Bd strains within the global
panzootic lineage (Lambertini et al. 2016; Becker et al.2017). Specifically, when averaging across host species, Bd from
Louisiana was most deadly, most likely to cause infection, and produced
the highest infection burdens (Figure 3 & S2). We also found
significant variation in mortality, prevalence, and pathogen load among
host species (Figures 3 & S2). Specifically, when averaging across Bd
strains, toads from Arizona and Tennessee had the highest mortality and
infection prevalence (Figure S2). Rapid mortality occurred in our
experiment when highly susceptible hosts were exposed to especially
virulent Bd strains. Specifically, toads from Arizona and Tennessee died
an average of 29 days sooner when exposed to Bd from Louisiana or Ohio
relative to any other novel host-pathogen interactions (Figures 3B &
S3). Further, our meta-analysis revealed that Bufonoidea species (toads
and relatives) were especially susceptible to Bd-induced mortality
compared to other host taxa, confirming previous research (Scheeleet al. 2019a) (Figure 3 & S2).
By combining a continental-scale factorial experiment with a
global-scale meta-analysis, we show that local host-pathogen
interactions typically resulted in higher host mortality, greater
infection success, and higher pathogen loads. However, we also found
that novel host-pathogen interactions do not always result in low
mortality, infection success, and pathogen loads. There was substantial
variation in novel host-pathogen outcomes, including pairings of
especially vulnerable hosts and especially deadly pathogen strains that
resulted in extremely rapid mortality. In fact, the host- and
strain-level effects accounted for more variation in our models than
strain novelty. Therefore, frequent introduction of novel strains
increases the risk of especially vulnerable hosts encountering
especially deadly pathogens despite pathogens being better adapted to
invade and replicate in local hosts. Therefore, we provide support for
both the local adaptation and naïve host syndrome hypotheses, highlight
how the two hypotheses are complementary rather than conflicting, and
emphasize the need for greater integration of these hypotheses and their
associated semi-disparate literature. Stochastic encounters between
deadly pathogen strains and vulnerable hosts will continue to rise as
human connectivity and encroachment on and degradation of wildlife
habitat increase. Thus, it is imperative that policy makers mitigate the
risk of pathogen spillover and dispersal (Altmann & Kolby 2017; Aguirreet al. 2021). Policies regarding surveillance, biosafety, and
security of wildlife and livestock trade that utilize One Health
approaches are especially promising for reducing risk (Cunninghamet al. 2017; Aguirre et al. 2021).