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.