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.