INTRODUCTION
Accelerating anthropogenic impacts are modifying habitats and disrupting
interactions between coevolved species (Barnosky et al. 2012),
including host-pathogen dynamics, raising concern for human and animal
health, biodiversity conservation, and ecosystem structure and function
(Jones et al. 2008; Wiethoelter et al. 2015; Allenet al. 2017; Rohr et al. 2019; Gibb et al. 2020).
However, given the complexity and ubiquity of anthropogenic impacts,
teasing apart the effects of perturbations on disease dynamics has
proven difficult. A key to solving this challenge is identifying how
human-induced stressors affect processes that mechanistically impact
epidemiological dynamics, such as host survival and fecundity and
pathogen infectivity (i.e., the ability of a pathogen to establish an
infection and replicate in a host).
Stressors affect transmission dynamics in three fundamental mechanistic
ways. First, when stressors reduce host survival and fecundity, they
reduce host density, and by extension, transmission of density-dependent
pathogens (McCallum et al. 2001). Second, host behavioral and
immunological traits that influence the acquisition, proliferation, and
dissemination of pathogens, a series of processes often summarized as
host competence (Barron et al. 2015). Host competence may
increase under stressful conditions that erode immune response to
pathogens (resource limitation or agrochemical exposure) (Knutieet al. 2017; Rohr et al. 2008). Third, stressors can have
direct and indirect effects on pathogens. Host condition can shape
pathogen fitness by mediating intra-host resource availability and host
immune response, as reviewed and modeled by Cressler et al.(2014). Pollution and environmental conditions may also negatively
affect pathogens, especially in free-living stages (Pietrock &
Marcogliese 2003). Given that these three distinct mechanisms predict
different outcomes, it is imperative to consider them collectively when
examining stress-mediated effects on disease dynamics.
We aim to synthesize the current understanding of how human-induced
stressors affect disease dynamics and consider the implications of these
stressors for mitigating disease emergence and threatened species
population declines. Here we define stress as any change that causes
actual or perceived threats to the homeostasis of an organism (pathogen
or host), precluding it from controlling fitness-critical variables
(Del Giudice et al. 2018). We began by reviewing the literature
to assess how stressors may affect host-pathogen interactions by
altering (1) host density, (2) host defenses, and (3) pathogen
infectivity. Further, we conducted a systematic search and meta-analysis
of studies where host fitness (host survival and fecundity) and pathogen
prevalence and intensity have been evaluated under benign and stressful
conditions (low resources, adverse environmental conditions, and
pollution) for infected and uninfected hosts. Given that host defenses
and pathogen infectivity are rarely evaluated independently, we used
infection prevalence and intensity to capture these two processes
(hereafter infectivity). Specifically, we evaluated how different types
of stressors affected host fitness and pathogen infectivity, if fitness
effects of stressors were more severe for infected vs. uninfected hosts,
and whether infectivity traits were more susceptible to stress than host
fitness traits.
To further synthesize our results, we incorporated our empirical
findings into two theoretical Susceptible-Infected (SI) models to
elucidate scenarios where infection rates were expected to increase or
decrease in response to the simultaneous trait changes (i.e., host
fitness and pathogen infectivity) occurring over resource and
environmental stress gradients. Our meta-analysis revealed similarly
negative responses of infected and uninfected hosts to stressors and
identified stressor type as determinant of infection outcomes. Our
results provide insights for predicting and mitigating the impacts of
stressor-pathogen interactions on human and animal health, more relevant
than ever, as human-induced perturbations are a growing threat
worldwide.