Stressor type modulates host fitness and infectivity in different ways
Our meta-analysis documented the dominant effects of stressors on host fitness and pathogen infectivity. Interestingly, we found that infected and uninfected hosts had proportionally similar sensitivity to stressors in relation to survival and fecundity. Furthermore, stressor type determined host fitness and pathogen infectivity outcomes. Although we found that resource limitation decreased host fecundity and pathogen intensity, other authors have described positive, negative, and unimodal relationships across animal taxa. For example, Cressler et al.(2014) found that as invertebrates increased their resource uptake, they increased their pathogen intensity, whereas increased resource consumption decreased pathogen intensity in vertebrates. They argued this differential response could be due to distinct immune systems and body sizes (Cressler et al. 2014). Contrary to their results, we found that both vertebrate and invertebrate hosts (which represented most of our data) reproduced less and carried a lower pathogen burden when facing limiting resources. One possible explanation is that hosts invest resources in immune defense at the cost of reproduction. In support of this hypothesis, it has been proposed that illness-mediated anorexia may enhance immune function by acting as a “master switch” that reduces investment in other physiological processes (Hite et al. 2020). For example, Cumnock et al. (2018) showed that malaria-infected mice reduced their food intake and switched from burning sugar (glycolysis) to fats (ketosis), which influenced host tolerance to infections. Alternatively, resource limitation could negatively affect pathogens, decreasing their capacity to reproduce within hosts. Lastly, resource-limited hosts are often smaller and may carry fewer pathogens, reducing pathogen intensity. This has been reported in the snail-Schistosome system, where smaller snails carry fewer parasites (Civitello et al. 2022). Moreover, inDaphnia populations, food shortage reduced body size with subsequent reductions in spore loads of a microsporidian parasite (Pulkkinen & Ebert 2004).
Regarding endogenous environmental stressors, we found that stressed hosts survive less but have higher pathogen intensity. Coping with fluctuating abiotic environments can be energetically demanding for hosts, and human activities may exacerbate the frequency and severity of naturally occurring fluctuations. For example, temperature variation occurs naturally, but climate change makes it unpredictable or more drastic (Harvell et al. 2002; Marcogliese 2008). When stressed, hosts may not resist infections (increasing pathogen proliferation) and/or compensate for damage done by the pathogen (tolerating infection), as seen when higher temperatures increase coral (Gorgonia ventalina ) susceptibility to fungus (Aspergillus sydowii ), while also increasing fungal growth and virulence (Wardet al. 2007).
Finally, we found hosts exposed to pollutants had higher mortality but lower pathogen prevalence. However, we note that these results must be interpreted cautiously, given that the experimental studies included in our meta-analysis intentionally used sub-lethal toxin doses. Low prevalence may be due to hosts dying before replicating and transmitting the pathogen. This result is consistent with mechanistic models of how toxicants influence pathogen transmission showing that infection prevalence was lower in more contaminated landscapes due to high host mortality (Sánchez et al. 2020). Although pollution can decrease parasitism if infected hosts suffer more than uninfected hosts from pollutant exposure, our analysis showed that hosts are equally sensitive to toxins regardless of infection status. Alternatively, parasites could also be negatively affected by pollution. For example, mortality increased in infected hosts as zinc concentration increased, but parasite burden peaked at intermediate zinc concentrations in a fish-parasite system (Gheorgiu et al. 2006). A follow-up study revealed that both parasite lifespan and fecundity were also negatively affected by zinc (Gheorgiu et al. 2007).