Evolutionary toxicology: Toward a unified understanding of life's response to toxic chemicals

The story of life on Earth is one of both ancient and ongoing evolution. All species on the planet today have in different ways evolved adaptations that promote fitness sufficiently well enough to sustain different metapopulations over long periods of time relative to the pace of environmental change. Indeed, species’ lifespans are estimated to be on the order of millions of years (Barnosky et al., 2011). At the same time, we now appreciate that evolution is a contemporary process that modifies traits and shapes fitness each and every generation (Carroll, Hendry, Reznick, & Fox, 2007; Hendry & Kinnison, 1999). As we show in this special issue, these two elements of evolutionary change— macroevolutionary diversification and contemporary evolutionary change—bear critical insights for ecotoxicology and point toward a fruitful integration of the fields of toxicology and evolutionary biology. Many adaptations that have arisen over macroevolutionary timescales reflect responses to selection imposed by toxins that characterized the early environment on the planet (Kirschvink & Kopp, 2008; Monosson, 2012; Tobler et al., 2011). Indeed, much of the early evolution of life, from its origins to the evolution of multicellular plants and animals, faced a central problem of evolving mechanisms for coping with toxicity imposed, for example, by heavy metals, ultraviolet light, oxygen, microbial toxins, and defensive chemicals produced by plants (Cockell, 1998; Coyle, Philcox, Carey, & Rofe, 2002; Kirschvink & Kopp, 2008; Rico, 2001). For modern ecotoxicology, evolutionary history suggests that in some cases, extant species may already possess preadaptations or adaptive capacity for dealing with exposure to toxicants (sensu Motychak, Brodie, & Edmund, 1999; Llewelyn et al., 2011). Further, closely related species may share similar tolerances to similar toxicants (Guénard, von der Ohe, de Zwart, Legendre, & Lek, 2011). Therefore, the evolutionary history of a given species or group of species may provide an important source of variation associated with tolerance to contaminants found in the environment today (e.g., Hammond, Jones, Stephens, & Relyea, 2012). This predictive capacity may be particularly true for historical toxins that have been remobilized as contaminants by recent human activities (e.g., via land use practices, agriculture, and mining). In contrast, adapting to novel contaminants such as synthetically produced chemicals with no precedent of occurrence in the environment may prove especially challenging, for example, if adaptive responses require novel genetic variation (Barrett and Schluter 2008). Moreover, the occurrence of contaminants alongside numerous other humaninduced selection pressures (e.g., climate change, ocean acidification, habitat conversion, commercial harvest) may further challenge the ability of organisms to adapt to environmental contaminants. After all, an individual’s fitness is influenced by the sum total of all stressors, which can act additively, antagonistically, and/or synergistically. In addition to the influence that macroevolution has had on species’ tolerance for toxins and toxicants, ongoing contemporary evolutionary change mediates tolerance over time periods relevant to policy and conservation. Although this view of evolution as a contemporary process has only recently become more prevalent in toxicology (Bickham, 2011), the awareness of the potential for organisms to adapt to environmental toxicants dates back to at least the early 20th century. At that time, Melander (1914) reported an experiment showing a reduced effectiveness of sulfurlime treatments on the agricultural pest Quadraspidiotus perniciosus (San Jose scale), a result contrasting the usual effect of complete mortality. This example appears to be the first reported evidence of pesticide resistance. Three decades later in 1945, with use of the miracle drug penicillin on the rise, Alexander Fleming saw fit to conclude his Nobel Lecture with a cautionary tale about the possibility of the evolution of antibiotic resistance, forewarning the inefficacy of treatment that would follow (Nobelprize. org). These early examples of resistance provided some of the first evidence that evolution can be quite rapid and that evolutionary change