INTRODUCTION
Human-induced environmental changes are altering the world at an
unprecedented rate, threatening the persistence of many animal and plant
species by modifying habitats and disrupting interactions between
coevolved species (Barnosky et al. 2012). These changes
underscore the importance of understanding how human actions impact
parasite dynamics in wildlife populations, as organisms that cause
disease are of concern to human and animal health, biodiversity
conservation, and ecosystem structure and function (Jones et al.2008; Wiethoelter et al. 2015; Allen et al. 2017; Rohret 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 become a major
challenge. 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).
A fundamental prediction of epidemiological theory is that high host
density promotes parasite spread (McCallum et al. 2001).
Therefore, is it reasonable to assume that stressors that impede
population growth, by reducing host survival and fecundity, will reduce
pathogen transmission. On the other hand, parasite transmission also
depends on behavioral and immunological traits of a host that influence
the acquisition, proliferation, and dissemination of parasites, a series
of processes often summarized as host competence (Barron et al.2015). However, hosts may become more competent under stressful
conditions that erode immune response to pathogens (i.e., resource
limitation or agrochemical exposure) (Knutie et al. 2017; Rohret al. 2008). Finally, stressors can have indirect and direct
effects on pathogens. Host condition is likely to shape pathogen fitness
by mediating intra-host resource availability (a bottom-up effect) and
host immune response (a top-down effect), as reviewed and modeled by
Cressler et al. (2014). In addition, pollution and environmental
conditions may also negatively affect pathogens, especially in
free-living stages (Pietrock & Marcogliese 2003). Considering these
three distinct mechanisms is imperative when examining stress-mediated
effects on disease dynamics, given that they predict different outcomes.
Our work aims to synthesize the current understanding of how
human-induced stressors affect disease dynamics and consider the
implications of these stressors concerning mitigating disease emergence
and threatened species population declines. Here we define stress as any
change that causes any actual or perceived threat to the homeostasis of
an organism, precluding it from controlling a fitness-critical variable
(Del Giudice et al. 2018). We begin by reviewing the literature
to assess the support of the primary mechanisms by which stressors may
affect host-pathogen interactions: by altering 1. host density, 2. host
defenses, and 3. pathogen infectivity. Further, we conduct a
meta-analysis of studies where impacts of 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 use infection prevalence and intensity to
capture these two processes (hereafter infectivity). Specifically, we
evaluated how the different types of stressors affect host fitness and
pathogen infectivity, if fitness effects of stressors are more severe
for infected vs. uninfected hosts, and if infectivity traits are more
susceptible to stress than host fitness traits.
To further synthesize our results, we incorporate our empirical findings
into two theoretical Susceptible-Infected (SI) models to elucidate
scenarios where infection rates are expected to increase or decrease in
response to the simultaneous trait changes occurring over resource and
environmental stress gradients. Our meta-analysis’ results support
similarly negative responses of infected and uninfected hosts to
stressors and identify stressor type as determinants for 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.