The competence of a species for a zoonotic disease can be broadly defined as its ability to cause new infections, thereby increasing the fitness of the causative parasite (Merrill and Johnson 2020). Because most zoonotic diseases originate from mammals, studies have sought to identify mammalian species likely to exhibit higher competence and the drivers that underlie variation in competence. Indeed, life-history theory has contributed greatly to how we understand disease competence across mammalian taxa. In particular, mammals that follow a faster pace of life (i.e., reproduction favored over survival), notably rodents, are considered more competent reservoirs for zoonoses (Plourde et al. 2017). Thus, a faster pace of life in mammals is associated with a higher competence for zoonotic diseases.

Globally, there has been a rise in the dissemination of chemical contaminants into the environment. In some instances, contaminants, such as pesticides, are intentionally introduced to remove a target species; but nontarget species are often exposed. Many species are able to develop resistance or tolerance to chemicals, which allows them to persist in contaminated environments. Species with such potential for adaptation are more likely to have a faster pace of life because they typically have larger populations, higher fecundity, and shorter generation times, which permits a greater standing genetic variation for selection to act on (Oziolor et al. 2020). Evidence for evolutionary responses to contaminants has been reported from faster-paced mammals, particularly rodents, such as anticoagulant rodenticide resistance in brown rats (Rattus norvegicus) and house mice (Mus musculus; McGee et al. 2020).

However, there are caveats to the proposed generalization that faster-paced mammals are more likely to evolve resistance or tolerance to chemical contaminants. Notably, because faster-paced species may show a higher sensitivity to chemicals, as a result of their larger surface area-to-volume ratios and faster metabolism, there could be a fundamental trade-off between the capacity for evolved responses and heightened sensitivity (Baas and Kooijman 2015). Consequently, if sensitivity is greater, extinction or reduction of populations may be the more likely outcome. If not, contaminated environments could then favor the persistence of faster-paced species with evolved tolerance or resistance mechanisms, a challenging issue already faced by pest management programs (e.g., rodenticides [McGee et al. 2020]).

Given that faster-paced mammalian species are likely to be 1) more competent reservoirs of zoonotic diseases and, 2) better able to evolve tolerance or resistance to chemicals, contaminated environments could ultimately favor the persistence of zoonotic reservoirs. Examples of such candidate species include brown rats and house mice, which can develop resistance to anticoagulant rodenticides while serving as highly competent reservoirs for various zoonoses (McGee et al. 2020).

Although chemical contaminants can alter disease competence (e.g., pesticides via suppressed immunity), there has been less focus on whether adaptive responses to contaminants can modify competence. Given that evolution of resistance or tolerance comes with biological trade-offs, the question arises if these accompanied trade-offs could inadvertently modify zoonotic reservoir competence, potentially changing the risk of disease spillover to humans. However, the likelihood of transforming into more competent zoonotic reservoirs may depend on whether the evolved response to chemical contaminants can cause a phenotypic switch that enhances rather than inhibits parasite fitness (Hua et al. 2017).

Although scant evidence from amphibian disease systems suggests that evolved tolerance to pesticides could modify disease competence (Hua et al. 2017), less is known about zoonotic disease systems from mammals. This knowledge gap has significant implications for public health and is very timely given the ongoing COVID-19 pandemic. In light of this uncertainty, we need further empirical information to address the proposed hypothesis that biological trade-offs from evolutionary responses to chemical contaminants have the potential to modify zoonotic reservoir competence and change disease spillover risk to humans.

Going forward, to address this challenging task, collaboration between those who study evolutionary toxicology and those who study infectious diseases could reduce individual expenses and effort, while allowing for the sharing of expertise across the spectrum of chemicals and parasites that can coexist in contaminated environments. Such an interdisciplinary approach may provide renewed perspectives and stimulate novel investigations that can lead to a comprehensive and predictive framework able to determine spillover risk depending on the host, parasite, or chemical in question. To best inform public health efforts in an increasingly polluted world, we need to expand the ways we understand and predict spillover from zoonotic reservoirs when evolved responses to chemical contaminants and their potential biological trade-offs are present.