Evolutionary Toxicology—An Informational Tool for Chemical Regulation?

Abstract

The Challenge:Evolutionary toxicology focuses on the drivers, mechanisms, and outcomes of pollution-driven genetic differentiation among populations. The focal questions address the types of chemical contamination acting as selective pressures; the genetics, epigenetics, and demography of impacted populations; as well as fitness costs and cross-resistances that may follow rapid adaptation. In this field, researchers incorporate tools from environmental chemistry, conservation genetics, population biology, and toxicology to understand the health and stability of impacted populations.Recent studies in evolutionary toxicology have illustrated diverse cases of population-wide adaptation to contamination (killifish, Hyalella, mosquitofish). Adaptation, by definition, is achieved through the localized loss of some individuals and genotypes and, thus, provides singular evidence of losses in biodiversity. Chemical regulations are generally supported by assessments that predict, largely through laboratory studies, the risks associated with chemical exposures. Evolutionary toxicology complements this approach by providing direct evidence of population and community impacts. Recent interest by the Society of Environmental Toxicology and Chemistry working group EVOGENERATE (Evolutionary and Multigenerational Effects of Chemicals) has launched discussions about the utility of evolutionary toxicology studies to inform chemical regulation. To further this discussion, one representative from each of 3 sectors, academia, government, and industry, was asked to provide opinions on the following questions:1) The considerable number of adaptive events reported in recent years suggests that current risk-assessment methods may not be exhaustive. What is risk assessment missing by not incorporating evolutionary toxicology endpoints to inform the regulation of toxic compounds? 2) Changes in the US Toxic Substances Control Act call for attention in 2 major aspects of predictive toxicology: organizational frameworks (e.g., adverse outcomes pathway) and fast screening methods (e.g., Omics, Tox21). Can evolutionary toxicology contribute to these advancements? 3) What needs to be done to make an evolutionary approach more accessible and useful to chemical regulation?

Trends in the Application of “Omics” to Ecotoxicology and Stress Ecology

“…Developments in these fields have been reviewed elsewhere [27][28][29][30][31][32][33]. Genomics studies in Evolutionary Toxicology that e.g., determine changes in allelic or genotypic frequencies caused by increased mutation rates are also covered elsewhere [34][35][36][37][38][39]. Included studies that utilized one or more of the following omics layers: transcriptomics, proteomics, metabolomics, and multiomics to study the effects of one or multiple stressors were classified based on (i) omics layer, (ii) studied species/taxa, and (iii) studied stressor(s).…”

Predicting Resistance: Quantifying the Relationship between Urban Development, Agricultural Pesticide Use, and Pesticide Resistance in a Nontarget Amphipod

“…Implications for Ecological Risk Assessment. The presence of adapted organisms is often considered evidence of ecological impairment, 25 and interest is building to use evolutionary toxicology to inform ecological risk assessment (e.g., Oziolor et al 24 ). The H. azteca system is unique because it involves an ecologically important nontarget species complex that has rapidly evolved to anthropogenic contamination with known molecular target sites and resistance alleles.…”

“…Although more research is needed to refine the extent of ecological impairment predicted by the presence of resistance H. azteca, the ecological risk assessment paradigm should support the move toward highthroughput genetic tools to assess risk. 24 At best, the increase in frequency of pesticide resistance alleles in H. azteca is an early warning system for aquatic ecosystems and, at worst, a contemporary indicator of wider pesticide-induced ecosystem damage.…”

“…Several amino acid substitutions, including those identified in H. azteca, provide highly specific protection against organochlorine, pyrethroid, or organophosphate insecticide compounds because they reduce the affinity and binding of the insecticide to its target site. 22,23 The frequent detection of independently evolved resistance alleles (M918L and L925I/V at the vgsc and G119S at ace-1) in multiple species within the H. azteca cryptic species complex serves as an indicator of ecological impairment, 24,25 although the full extent of that impairment has not yet been elucidated. The consideration of H. azteca pesticide resistance mutation data in the ecological risk assessment paradigm is an important next step for evolutionary toxicology and has already proved useful in vivo for discriminating among sources of toxicant stress.…”

Integrating Evolved Responses to Chemical Contaminants with Zoonotic Reservoir Competence

“…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).…”