Introduction
Human-facilitated pathogen dispersal (often termed pathogen pollution)
has led to an increase in emerging infectious diseases over the last few
decades (Cunningham et al. 2017) and is a major threat to global
biodiversity and food security. Introduced pathogens can cause
catastrophic animal (e.g. crayfish plague, avian malaria) and plant
(e.g. chestnut blight, citrus greening) declines and economic losses
(Daszak et al. 2000; Anderson et al. 2004). Pathogen
pollution is also a primary threat to public health, as it has
contributed to several recent deadly epidemics and pandemics (e.g. SARS
CoV2) (Daszak et al. 2000; Morens et al. 2020).
Understanding how hosts respond to novel pathogens is necessary to
predict and prepare for outbreaks of emerging pathogens, which are on
the rise globally (Cunningham et al. 2017). However, there is a
set of seemingly contradictory hypotheses on novel pathogens in the
literature. The naïve host syndrome hypothesis asserts that hosts are
especially vulnerable to novel pathogens because hosts have lower
evolved immunological defenses against these pathogens, resulting in
high host mortality and host population suppression (Carey et al.1999; Anderson et al. 2004; Taraschewski 2006; McKenzie &
Peterson 2012; Lymbery et al. 2014). In contrast, there is also a
very rich literature indicating that pathogens are generally better
adapted to infect and replicate in local rather than novel host species
(Lively & Jokela 1996; Gandon & Van Zandt 1998; Kaltz & Shykoff 1998;
Lively & Dybdahl 2000; Torchin et al. 2003; Torchin & Mitchell
2004; Morran et al. 2011; Strauss et al. 2012; Lymberyet al. 2014; Parker et al. 2015; Bolnick & Stutz 2017;
Johnson et al. 2021). Hence, the naïve host syndrome suggests
that pathogens are able to invade novel hosts because of a lack of
co-evolutionary history, whereas local adaptation suggests that
pathogens are better able to invade local hosts because of their
co-evolutionary history (Lively & Jokela 1996; Gandon & Van Zandt
1998; Kaltz & Shykoff 1998; Lively & Dybdahl 2000; Torchin et
al. 2003; Torchin & Mitchell 2004; Morran et al. 2011; Strausset al. 2012; Lymbery et al. 2014; Parker et al.2015; Bolnick & Stutz 2017; Johnson et al. 2021) (Figure 1).
Rarely do local adaptation and naïve host syndrome studies cite one
another or acknowledge their ostensibly mixed messages.
Here, we hypothesize that pathogens are generally better adapted to
infect and replicate in local hosts, resulting in deadlier host-pathogen
outcomes. However, we also hypothesize that enough variance exists in
novel host-pathogen outcomes to pose substantial risk that an especially
virulent host-pathogen combination will occur given sufficient pathogen
introduction events (Torchin & Mitchell 2004; Lloyd-Smith et al.2005; Reeder et al. 2012; Cohen et al. 2018; Golaset al. 2021). Thus, we postulate that pathogen pollution is
dangerous because, as pathogen introductions occur with increasing
frequency, the probability increases that (i ) a particularly
deadly strain of a pathogen will devastate a naïve host population,
(ii ) a particularly vulnerable host population will be exposed to
a new pathogen, and (iii ) especially virulent host-pathogen
combinations will occur (Fig. 1). Researchers might be biased towards
the assumption that novel pathogens are often devastating because they
predominantly only observe pathogen introductions that establish and are
problematic, even though most introductions might fail because of a lack
of co-evolutionary history (Torchin et al. 2003; Torchin &
Mitchell 2004).
Amphibian-Batrachochytrium dendrobatidis (Bd) interactions are
ideal to address these hypotheses for several reasons. Bd spread
globally in the early 20th century, possibly with the
expansion of trade (O’Hanlon et al. 2018), and thus is an
invasive pathogen in much of its range with host-parasite outcomes that
vary greatly in virulence. Bd represents one of the most urgent
ecological disasters on the planet as it is implicated in the declines
and extinctions of over 500 amphibian species around the globe (Scheeleet al. 2019b) and can even adversely affect co-occurring
non-amphibian species (Brannelly et al. 2012; McMahon et
al. 2013; Nordheim et al. 2021). Further, Bd is considered
endemic in many regions (Venesky et al. 2014), with some evidence
that this endemicity is driven by amphibian hosts adapting to local Bd
strains (Voyles et al. 2018; Waddle et al. 2019; Fisher &
Garner 2020; McDonald et al. 2020). While many host-pathogen
systems exhibit a trade-off between virulence and transmission, field
and laboratory evidence suggest transmission is not significantly
limited by virulence, at least in part due to non-amphibian reservoir
hosts (Fisher et al. 2012; McMahon et al. 2013). Further,
high Bd loads lead to greater host mortality, suggesting that mortality
is likely a suitable measure for pathogen performance in this system
(Greischar & Koskella 2007; Fisher et al. 2012; Fu & Waldman
2019; Scheele et al. 2019b).
To test the hypotheses described above, we identified six populations of
toads from across North America (Arizona, California, Louisiana, Ohio,
Tennessee, and Quebec, Canada; Table S1) and, in a “common-garden”
experiment, measured host mortality and infection prevalence and
abundance when the toads were exposed to their local strain of a chytrid
fungus, Batrachochytrium dendrobatidis (Bd), five non-local
strains, and a sham control (Table S2). We define a novel strain as one
that is not from the same host population. To complement the
common-garden experiment, we assembled a host mortality dataset of 84
experiments from 26 Bd studies that included 23 amphibian species, 22
unique Bd strains, and wide variability in local and novel host-parasite
interactions. Using this dataset, we conducted a global-scale
meta-analysis to test for evidence of local adaptation, particularly
susceptible host populations, and especially deadly Bd strains and
host-Bd strain combinations.