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

Evolutionary Applications2017Vol. 10(8), pp. 745–751

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Steven P. Brady, Emily Monosson, Cole W. Matson, John W. Bickham

Abstract

Darwin himself could scarcely have found a better example of the operation of natural selection than is provided by the way the mechanism of resistance operates. Carson, 2002 Over the course of billions of years, receptors and the organisms in which they function have been evolving endocrine systems that are astonishing in their complexity, diversity, and biological importance. Protecting the life forms and ecosystems that have emerged from this evolutionary process will require that our policies take account of these characteristics. Thornton, 2003 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 meta-populations 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 pre-adaptations 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 re-mobilized 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 human-induced 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 sulfur-lime 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 can have important ramifications for human health and the economy (Palumbi, 2001). By the middle of the 20th century, more formal evidence for evolutionary responses to a diversity of toxicants began to mount, with reports of pesticide resistance on the rise. Indeed, in her renowned book, Rachel Carson devoted an entire chapter of Silent Spring to the evolution of pesticide resistance (2002). Around that time, in addition to numerous reports of invertebrates and plants evolving pesticide and industrial contaminant resistance (e.g., Antonovics, Bradshaw, & Turner, 1971; Keiding & Van Deurs, 1949; March & Metcalf, 1949), some of the first examples of toxicant resistance in vertebrates were beginning to emerge. While artificial selection experiments demonstrated the capacity for increased tolerance to DDT in mice (Ozburn & Morrison, 1962), studies of wild populations indicated that resistance was evolving in nature. For instance, Boyle (1960) showed that a rat population on a farm in Scotland had evolved resistance to two different poisons (warfarin and diphacinone). Around the same time, multiple populations of frogs and fish had evolved resistance to DDT and other insecticides applied to farm fields (Boyd & Ferguson, 1964; Boyd, Vinson, & Ferguson, 1963). As these examples of resistance grew, it was beginning to look like our industrial age chemicals and cures were contributing to a new phenomenon: rapid evolution in response to toxic chemicals mobilized by human activities. Yet for much of the twentieth century, these early examples of resistance to pesticides and antibiotics had been set aside from mainstream evolutionary biology, considered instead to be special cases of evolution acting unusually rapidly. Recently, however, this view of evolution has changed. It is now clear that these early accounts of resistance were not exceptional cases of fast evolution. Rather, these examples were just the beginning of what is sometimes referred to as the “newest evolutionary synthesis,” reflecting our recent understanding that contemporary evolutionary changes—those occurring in just a few generations—are common and widespread (Hendry, Gotanda, & Svensson, 2017; Schoener, 2011). While such changes have been detected in natural contexts such as in response to variation in food resources (Grant & Grant, 2002) or predation pressures (Reznick, Shaw, Rodd, & Shaw, 1997), many recent examples have emerged in human-modified contexts (Carroll et al., 2014; Hendry et al., 2017; Smith & Bernatchez, 2008), including climate change (Norberg, Urban, Vellend, Klausmeier, & Loeuille, 2012), land conversion (Alberti et al., 2017; Brady & Richardson, 2017), invasive species (Novak, 2007), and commercial harvest (Heino, Díaz Pauli, & Dieckmann, 2015). Recently, we have also developed a greater awareness of a role for toxic chemicals in contemporary evolution, including the capacity of toxins and toxicants to mediate genetic change, plasticity, and epigenetic effects. As a result, our view of toxic chemicals has shifted, such that we are no longer limited to assessing chemicals exclusively for their acute or chronic intragenerational toxic effects. Instead, we increasingly see the potential for toxic chemicals to cause transgenerational effects mediated, for example, by natural selection. Undoubtedly, the emergence of industrial era chemicals has created—and continues to create—profoundly different selective environments for organisms on the planet today. Indeed, there now exists an amazing diversity of industrial chemicals. For instance, the Toxic Substance Control Act Chemical Substance Inventory lists over 85,000 chemicals on the U.S. market (U.S. Government Accountability Office 2013). Coupled with the extraction and global redistribution of chemical and radioactive elements, minerals, and compounds once found primarily within Earth's crust (e.g., mercury, lead, cadmium, uranium, hydrocarbons), the combined novelty, intensity, and scope of modern day contaminants are, as best we can tell, unprecedented. The extent to which evolution will contribute to the success of populations facing this new suite of pressures remains uncertain. Attempting to understand this capacity of evolution is a recurrent theme in the papers appearing in this special issue (see especially Whitehead et al. 2017). Our ability to gain this understanding will surely improve as we broaden our assessment of evolutionary toxicology beyond the scope of pesticide resistance, and focus on increasingly diverse contexts where nontarget organisms are impacted by the use and distribution of toxic chemicals in the environment (e.g., Hua et al. 2017; Whitehead, Clark, Reid, Hahn, & Nacci, et al. 2017). Indeed, numerous observations of phenotypic and molecular changes have now been described in wild populations exposed to industrial age chemicals. These changes are diverse, ranging from the evolution of phenological traits to desensitization of aryl-hydrocarbon receptors to increased DNA mutation rates to epigenetic effects (Bélanger-Deschênes, Couture, Campbell, & Bernatchez, 2013; Bickham, 2011; Bickham, Sandhu, Hebert, Chikhi, & Athwal, 2000; Crews & Gore, 2012; Kiang, 1982; Oziolor, Bigorgne, Aguilar, Usenko, & Matson, 2014; Oziolor & Matson, 2015; Reid et al., 2016; Yauk, Fox, McCarry, & Quinn, 2000). Notably, however, not all changes are adaptive. Rather, it appears that in some cases, populations can evolve maladaptive responses to contaminants (e.g., Brady, 2013; Rogalski, 2017; Rolshausen et al., 2015). For example, strong selection pressures such as those from contaminants can reduce population size and lead to inbreeding depression or drift (sensu Falk, Parent, Agashe, & Bolnick, 2012). Moreover, contaminant-induced selection can reduce genetic variation, which can limit capacity for adaptive responses to future stressors. Together, these various biological changes induced by toxic chemicals highlight the complexity of outcomes that we can begin to understand when evolution is considered in the context of ecotoxicology. Solidifying the field of evolutionary toxicology should help resolve these complexities as we continue to elucidate the relationships between toxic exposure, genetic architecture, molecular pathways, trait variation, and population responses. Indeed, it is our hope that this special issue will not only showcase the recent advances in ecotoxicology availed by evolutionary perspectives but also catalyze a more unified field of study that routinely considers the role of evolution in governing life's responses to toxic chemicals. Having emerged in response to the need for human health and environmental regulatory policies, toxicology as a field has been the workhorse science of numerous industries and regulatory agencies (Monosson, 2005). In fact, one hypothesis concerning the field's development is that the “discipline expands in response to legislation” (Gallo & Doull, 1996). And yet there currently exists little if any consideration of evolution in policymaking or regulatory processes relating to environmental contaminants. However, as reports of resistance to antibiotics, insecticides, herbicides, and other industrial age chemicals rise, the relevance of evolutionary responses to toxic chemicals should become increasingly apparent. For instance, failing to consider the influence of evolutionary responses to toxicants can result not only in quantitative error but also qualitatively different inferences (Brady & Richardson, 2017; Oziolor, De Schamphelaere, & Matson, 2016). As well, by failing to consider the evolutionary history of biological systems involved in defending life from natural toxins (e.g., Goldstone et al. 2006), we may miss opportunities to predict how life might respond to industrial age chemicals that interact with these systems. As interest in evolutionary toxicology begins to rise (Coutellec & Barata, 2011, 2013), the time is ripe to examine the breadth of this foundational perspective. Elements of evolutionary biology have started to become utilized in various aspects of toxicology. For example, theoretical and analytical studies have developed and incorporated evolutionary techniques for ecotoxicology (e.g., Bélanger-Deschênes et al., 2013; Klerks, Xie, & Levinton, 2011) while conceptual studies have developed frameworks for integrating evolution and ecotoxicology (e.g., Leung et al., 2017). Empirical studies have increasingly been detecting evolutionary responses in diverse environmental contexts, for example, in response to mining effluents and industrial pollutants (Bougas et al., 2016; Chen et al., 2015; García-Balboa et al., 2013; Laporte et al., 2016; Reid et al., 2016). Studies are also beginning to show that adaptation to toxicants can evolve at a cost, for example, in the form of increased sensitivity to oxidative stress following adaptation to PCBs (Harbeitner, Hahn, & Timme-Laragy, 2013). As a result, we are beginning to appreciate that potential consequences of adaptation should be carefully considered when evaluating the potential for evolution to mediate current and subsequent environmental impacts. Despite these recent efforts to draw upon and promote evolutionary perspectives in ecotoxicology, the various insights and ideas found in the literature remain fragmented. That is, although there have been various efforts at unifying evolutionary and ecotoxicological approaches toward a more holistic understanding of toxicity, ecotoxicology still largely lacks an evolutionary perspective. Indeed, it was our perception of this disconnect that motivated us to compile this special issue. As we began searching for potential contributions, we found relatively few researchers actively integrating toxicology and evolution. Our goal with this special issue is to bring together and showcase these diverse perspectives, approaches, and insights under one broad umbrella of evolutionary toxicology. In doing so, we hope to cultivate a more fruitful pursuit toward the understanding and mitigation of the negative biological and ecological impacts of chemical contaminants. As with other applied fields strengthened with evolutionary perspectives (e.g., medicine, public health, agriculture, conservation biology), we feel that embracing a heightened awareness of the influence of evolutionary processes on life's response to toxic chemicals will provide with a understanding that capacity for the consequences of contaminants on and At the same time, the of evolutionary the applied field of toxicology should provide to evolutionary biology. evolutionary in toxicology should lead not only to more of contaminant exposure but should also the of systems in which to study evolutionary processes and outcomes (Monosson, and in the interest in understanding evolution in human-modified environments (Alberti et al., 2017; Hendry et al., 2017). Moreover, with rapid advances of in and other it is that evolutionary toxicology will insights beyond what we can today Bickham, & Matson, 2017). In this special issue, Whitehead et al. insights from a example of contemporary evolution, in which wild populations of have to some of the in the The how of their genetic architecture, and of contaminants may be in the for adaptive responses enough to promote population The that genetic variation may have been a a adaptive response populations in the that evolution may only be a fast enough to In example of contemporary evolution in a et al. the adaptation of populations of the common in response to the as the in U.S. this is estimated to have of the of 2012). The by et al. is quite in that the populations and the the showed evidence of adaptive evolution, indicated by rapid development and an increased tolerance to relative to populations to the However, a selection experiment for to the field showing the evolution of development time, but not of tolerance to These that rapid evolution of tolerance could take in response to the toxic effects of but require more time or more genetic variation than was in the selection mechanisms are increasingly considered as transgenerational responses to environmental stressors. et al. and also the by the of to the potential of both genetic and epigenetic changes in common has a as to various forms of environmental and this like the has been for phenotypic and genetic a of the genetic and epigenetic of populations of the genetic in response to exposure, but were to epigenetic between exposed and the field of particularly as it may to transgenerational responses to environmental In Oziolor et al. how approaches provide to the assessment of populations under chemical particularly when to impacts. is as an to the of evolutionary described by with an on new of study by and et al. that two different contaminants can adaptive evolutionary in a an evolution the show that can evolve life in response to but life in response to they also found that populations exposed to both toxicants in evolved similar or fitness to populations evolving in response to of the toxicants in Moreover, evolution in response to this toxicant not reduce fitness in the adaptation to toxicants not a fitness to a This further the complexity of responses and future consideration of the processes that may limit fitness in the contexts of environments with exposure Notably, they on two and are in the environment as a result of human activities. In Hua et al. recently evolved pesticide tolerance in an is to influence its to Notably, adaptation to pesticides can in some cases adaptive the show that adaptation to a pesticide is with resistance to a common However, the also show that adaptation to a pesticide can as indicated by increased following exposure to This from Hua et al. the need to consider multiple in evolutionary ecotoxicological and us of the of nontarget species in agricultural contexts, where of our about evolution has been limited largely to studies of pest important from Hua et al. is that context when assessing the evolutionary impacts of contaminants on a given a point considered in ecotoxicology. Hua et al. bring a much to evolutionary toxicology. This special issue also insights how the of evolutionary in ecotoxicology can both and Brady, Richardson, and the evolutionary history of responses to stressors, on the toxicity of an ancient and a modern and the potential capacity of organisms to adapt to By a of tolerance the highlight the potential of evolutionary relationships in species’ responses to Brady, Richardson, and also point that contemporary evolution may result in in contaminant tolerance with the of between populations that between that these are to over time, contemporary evolutionary perspectives may our perception of the of for is a and toxicant as as the While defensive responses to and as DNA and at the of life and have been for over years, has recently the with and et al. the consequences of exposure in wild on a study they found increased genetic diversity in populations environments the conclude that an in the mutation was by exposure in This suggests that toxicants can not only lead to reduced genetic diversity by acting as of natural selection but can also mutation rates and the possibility for novel adaptive and maladaptive genetic variation (e.g., genetic or set the plants have been for This predation may in the diversity of of recent and on considers how some chemicals share with the potential to interact with endocrine systems. evidence suggests that exposure of vertebrates to such can influence and and how exposure of vertebrates to may not only selection but also opportunities for vertebrates to from these chemicals. This a view of how ecological and can mediate the toxicity of a given The in this special issue provide both an and a current of evolutionary understanding and in ecotoxicology. hope this will draw to and the of evolutionary approaches in ecotoxicology, awareness of the efforts of these two fields in that they will to each For example, an evolutionary might consider the of industrial chemicals on the development of the toxic response in and in there examples of periods in the evolutionary (e.g., natural yet in the chemical and can we the evolution of tolerances to different contaminants we draw on our current and future understanding of evolution to help genetic and mechanisms that are particularly or to of focus on evolutionary history may also provide insights the of life's response to this in us to better use of and molecular approaches in All of which may be as to chemicals that effects. And as and are now faced with and this of would a understanding of the of these systems help us or yet in what of other populations that like various species of fish have to toxic environments (e.g., et al., 2011; Bélanger-Deschênes et al., 2013; Whitehead et al. these examples the or or in is ripe for a both evolutionary and the evolutionary of life's defensive systems and to our capacity to understand and the biological impacts of toxic chemicals. The understanding that has been in evolutionary biology and ecotoxicology critical for both Indeed, a greater between these will lead to a more holistic understanding of the ways that organisms respond to contaminants in the toxicology how the of evolutionary can applied toxicology and ecotoxicology. of understanding hope that this special issue will a new generation of motivated by the influence that evolution has had and can have on the ways that organisms respond to and with natural and environmental contaminants. Bernatchez, Hendry, and for and about this special issue. are to and for their in and this issue.

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