Evolutionary toxicology: Meta-analysis of evolutionary events in response to chemical stressors

Abstract

The regulatory decision-making process regarding chemical safety is most often informed by evidence based on ecotoxicity tests that consider growth, reproduction and survival as end-points, which can be quantitatively linked to short-term population outcomes. Changes in these end-points resulting from chemical exposure can cause alterations in micro-evolutionary forces (mutation, drift, selection and gene flow) that control the genetic composition of populations. With multi-generation exposures, anthropogenic contamination can lead to a population with an altered genetic composition, which may respond differently to future stressors. These evolutionary changes are rarely discussed in regulatory or risk assessment frameworks, but the growing body of literature that documents their existence suggests that these important population-level impacts should be considered. In this meta-analysis we have compared existing contamination levels of polychlorinated biphenyls (PCBs) and polycyclic aromatic hydrocarbons (PAHs) that have been documented to be associated with evolutionary changes in resident aquatic organisms to regulatory benchmarks for these contaminants. The original intent of this project was to perform a meta-analysis on evolutionary events associated with PCB and PAH contamination. However, this effort was hindered by a lack of consistency in congener selection for "total" PCB or PAH measurements. We expanded this manuscript to include a discussion of methods used to determine PCB and PAH total contamination in addition to comparing regulatory guidelines and contamination that has caused evolutionary effects. Micro-evolutionary responses often lead populations onto unique and unpredictable trajectories. Therefore, to better understand the risk of population-wide alterations occurring, we need to improve comparisons of chemical contamination between affected locations. In this manuscript we offer several possibilities to unify chemical comparisons for PCBs and PAHs that would improve comparability among evolutionary toxicology investigations, and with regulatory guidelines. In addition, we identify studies documenting evolutionary change in the presence of PCB and PAH contamination levels below applicable regulatory benchmarks.

Evolutionary toxicology in an omics world

“…Effects such as (i) genome-wide changes in diversity, (ii) changes in allelic or genotypic frequencies due to contaminant-mediated selective pressure, (iii) changes in gene flow between populations, and (iv) increased mutation rates (Bickham, 2011) have been used to describe and search for patterns of differentiation. Studies in this field explore a wide range of selective pressures: metals (Xie & Klerks, 2003), polycyclic aromatic hydrocarbons Ownby et al, 2002), polychlorinated biphenyls (Nacci et al, 1999;Oziolor, Bigorgne, Aguilar, Usenko, & Matson, 2014), dioxins and furans (Yuan, Courtenay, Chambers, & Wirgin, 2006), and in addition a variety of organisms (Oziolor, De Schamphelaere, & Matson, 2016a), but mostly focused on aquatic species. Previous reviews in the field focus on evolutionary research in fish (Wirgin & Waldman, 2004), across stressors (Oziolor & Matson, 2015), and the push toward quantitative genetics to link these processes to heritability and fitness of populations (Klerks, Xie, & Levinton, 2011).…”

“…As evolution to contamination results from generations of elevated mortality or reproductive effects, there are current efforts to relate evolutionary toxicology studies to regulatory limits in aquatic environments (De Coninck, Janssen, & De Schamphelaere, 2014;Oziolor et al, 2016a). Currently, regulatory limits are driven by standard toxicological end points, such as mortality and changes in reproduction (Long, Field, & MacDonald, 1998;MacDonald, Ingersoll, & Berger, 2000).…”

“…On the other hand, considering that adaptation to contaminated environments is a result of such changes occurring over multiple generations, it seems that evolution can inform regulation and risk analysis. Meta-analyses use studies in which population adaptation has occurred and compare the contamination levels measured in these environments to regulatory benchmarks (De Coninck et al, 2014;Oziolor et al, 2016a). These studies are complicated by the use of different numbers and mixtures of chemical congeners between evolutionary studies and those used to set regulatory limits (Oziolor et al, 2016a).…”

“…Meta-analyses use studies in which population adaptation has occurred and compare the contamination levels measured in these environments to regulatory benchmarks (De Coninck et al, 2014;Oziolor et al, 2016a). These studies are complicated by the use of different numbers and mixtures of chemical congeners between evolutionary studies and those used to set regulatory limits (Oziolor et al, 2016a). Even with this limitation, researchers have documented evolutionary adaptation in environments with contamination levels below relevant regulatory benchmarks (Oziolor et al, 2016a).…”

“…These studies are complicated by the use of different numbers and mixtures of chemical congeners between evolutionary studies and those used to set regulatory limits (Oziolor et al, 2016a). Even with this limitation, researchers have documented evolutionary adaptation in environments with contamination levels below relevant regulatory benchmarks (Oziolor et al, 2016a). Such conclusions open the discussion for a more thorough discourse between evolutionary toxicology and environmental regulation.…”