Genetics And Ecotoxicology

Valery E. Forbes, Valery E. Forbes

• Publisher: CRC Press
• Year: 2022
• ISBN:
  9781000162974
• Edition: 1
• Topic: Sciences biologiques
• Subtopic: Génétique et génomique

This first volume in the series provides a detailed treatment in ecotoxicology and stresses why genetics is important in understanding if and how chemical contaminants affect populations. Written by an array of international contributors from various fields covering mammals, invertebrates, fish, plants, as well as molecular ecotoxicology, this book considers both ecological/evolutionary consequences and practical implications of the interplay between chemical toxicants and the genetic population.
In broadening the understanding of ecological response, this resource ranges from molecular to classical genetics, from plant to animal, from asexual to sexual, touching on some fundamental issues of evolutionary biology. In addition, gaps in our present understanding of genetic and ecotoxicological processes and future research directions have been identified.

1 Genetics and Ecotoxicology—Insights from the Interface

Valery E. Forbes

10.4324/9781003075431-1

Abstract. The ten contributions to this volume address a number of key issues that, taken together, summarize our current understanding of the relationship between genetics and ecotoxicology. They do so from very different perspectives—they examine different taxonomic groups and contaminant classes, use different methodological techniques, and approach their questions using a variety of theoretical and empirical approaches. What emerges from an analysis of these contributions are some important, and a few surprising, conclusions that bear on the consequences of toxicant exposure for genetic variability, the importance of genetic variation in determining organism responses to toxicants, and the extent to which the study of genetic variation has a role to play in ecological risk assessment. In addition, gaps in our present understanding of genetic and ecotoxicological processes have been identified that suggest important challenges for future work in these fields.

Keyword. Adaptation, genetic variability, molecular damage, risk assessment

Implications of Exposure to Toxicants for Genetic Variability

Much of the literature dealing with the potential effects of toxicant exposure on the genetic variability of natural populations has been based on two major concerns. The first concern is that exposure to toxicants may cause reductions in the amount of genetic variability in populations, which will lead to a loss of adaptability and hence increase the probability of population extinction. The second concern is that exposure to toxicants may select for resistant genotypes and that, possibly as a result of various costs associated with tolerance, such genotypes have reduced fitness (relative to nonresistant genotypes) in the absence of exposure. Clearly, if either or both of these concerns are justified, the long-term ecological and evolutionary implications are serious. It is therefore critical to evaluate the extent to which empirical evidence has been produced in their support.

As summarized by Gillespie and Guttman (chapter 4), many studies have reported reductions in allozyme variation in populations from contaminated habitats. But as these authors point out, changes in allozyme frequencies (even if selected by toxicant exposure) do not necessarily indicate negative consequences for the population at hand. They argue that only if the changes in allozyme frequencies are associated with reduced average heterozygosity or with reduced fitness should the allozyme changes be considered negative. In their studies they were able to demonstrate a link between allozyme frequency and tolerance to pollutants. However, the evidence that such allozyme changes were associated with negative impacts on populations is less clear.

Snell et al. (chapter 9) use simulation models to directly address the issue of genetic diversity loss via selection and drift at nonselected loci in rotifer populations. They found that heterozygosity loss due to toxicant-caused reductions in population growth rate were minimal. Rather than loss of genetic diversity per se, the most serious consequence of reduced population growth rate was a reduction in resting egg production. Resting eggs, which are produced sexually, may remain dormant for several years under environmental conditions that would be lethal to adults. Thus, the production of resting eggs by cyclical parthenogens such as rotifers is crucial for allowing populations to become reestablished after periods of environmental stress. Also, it appears that sexual reproduction is inhibited at lower toxicant concentrations than is asexual reproduction in these animals.

Negative effects associated with the adaptation of chironomid populations to cadmium included increased mortality and larval development time in clean conditions (Postma and Groenendijk, chapter 5). However, gene flow from adjacent nonadapted populations had an important influence on the evolution of tolerance in exposed populations and contributed to maintaining their genetic diversity.

Selection against tolerant plant genotypes has been shown to occur on uncontaminated soils, consistent with the idea that there are costs associated with tolerance (Shaw, chapter 2). However, as Shaw points out, the evidence for costs of tolerance is indirect, and the exact nature of such costs remains poorly understood. Again, gene flow between tolerant populations and adjacent nontolerant populations can have an important influence on population genetic structure and diversity.

In chapter 3 (Weis et al.), a single species-toxicant combination, Fundulus heteroclitus and mercury, is used to demonstrate the potential complexities that may provide difficulties in identifying the existence and genetic basis of tolerance. For example, the authors found that fish embryos from an exposed site exhibited increased tolerance to mercury, whereas larvae and adults from this site did not. These authors and others have performed extensive allozyme analyses of this species along the Atlantic coast of the United States, and although different subspecies were identified, genetic markers clearly associated with pollutants and enhanced tolerance could not be detected. Nor were there indications from these extensive studies that tolerant populations are less genetically diverse than their nontolerant conspecifics.

At the community level, severely polluted habitats are often less species rich and in this sense have a lower genetic diversity than unpolluted habitats. However, the evidence that toxicant exposure reduces genetic variability at the population level and is accompanied by reductions in the adaptability of toxicant-resistant populations is weak. Negative effects on fitness-related traits have been observed in tolerant populations in some cases (e.g., Shaw, chapter 2; Gillespie and Guttman, chapter 4; Postma and Groenendijk, chapter 5), but not others (e.g., Shaw, chapter 2; Gillespie and Guttman, chapter 4). Evidence that toxicants select for particular life-history traits, such as earlier age at maturity (e.g., Weis et al., chapter 3) can have positive effects on population growth rate and could provide a mechanism for the spread of tolerant genotypes into adjacent uncontaminated habitats.

Much of the evidence for selection against tolerant genotypes derives from cases in which exposures have been extreme. For species in which tolerant genotypes have evolved—and even in those cases in which selection against tolerant genotypes in adjacent uncontaminated sites has been demonstrated—there are no cases in which the evolution of tolerance has resulted in the decline of the species. Largely, this appears to be due to extensive gene flow from uncontaminated sites.

Although most concern has focused on decreases in genetic diversity as a result of toxicant exposure, Klerks (chapter 6) notes that exposure to certain toxicants may increase genetic diversity as a result of increased mutation rate. In addition, Gillespie and Guttman (chapter 4) point out that toxicant-caused reductions in population size can increase, as well as decrease, the frequency of rare alleles. Most of what we know about the consequences of toxicant exposure for the evolution of tolerance is based upon single toxicants acting in isolation, and the majority of studies have concerned either heavy metals or pesticides. Using a combination of theoretical and empirical approaches, Klerks considers how contaminant complexity is likely to influence the evolution of tolerance. He argues that exposure to a mixture of contaminants may reduce selection intensity for the individual toxicants, thereby reducing the likelihood of tolerance evolution. This argument is supported by studies of pesticide and antibiotic resistance in which combinations of independently acting toxicants have proved effective in slowing down the development of resistance in the target species. However, as Klerks points out, failing to detect tolerance in exposed populations can be due to a number of factors, and great care must be taken when discounting possible explanations. The fact that contamination of natural habitats frequently involves mixtures of substances emphasizes the importance of exploring whether the genetic consequences of exposure to complex mixtures differ from those occurring in response to single toxicants.

Implications of Genetic Variation for Responses to Toxicants

It has long been recognized that the existence of genetic variation for tolerance is a prerequisite for the evolution of tolerance. Evidence for genetic variability in tolerance to toxic chemicals is widespread, as reviewed by a number of the authors in this volume. Less is known about the specific genetic basis of tolerance and the degree to which it is influenced by the level and duration of exposure. A long history of studies of plants growing in metal-contaminated habitats suggests that the presence of tolerance is controlled by a limited number of major genes in combination with modifier genes that influence the level of tolerance (Shaw, chapter 2). However, much of this work deals with contamination that has been abrupt and severe, and it may be that gradual, low-level contamination results in a different set of genetic consequences.

Genetic variation has posed difficulties for ecotoxicologists in that it has been associated with substantial differences in the phenotypic responses of different populations to toxicant exposure. Such variability in toxicant responses complicates attempts to extrapolate biological effect concentrations from standardized laboratory test results to nature. A main concern in this regard is that we may be under-protecting certain populations to the extent that sensitive genotypes are not accounted for. Not only do many of our standard laboratory tests employ populations having little or no genetic variability (e.g., clones), but there is evidence (discussed by Baird and Barata, chapter 11) that the genotypes used for standard tests may be more tolerant than average, possibly yielding biological effect concentrations that are even less protective than recognized.

Although genetic variation is generally believed to be important in determining the responses of populations to toxicants, the existence of genotype x environment interactions prevents broad generalizations as to the relative importance of genetics versus environment. Forbes et al. (chapter 10) found that genetic variability among clones ofAnemia played a minor role in controlling the response of these organisms to copper exposure. In contrast, studies by Baird and colleagues have demonstrated that genetic differences in tolerance to toxicant exposure can, in some cases, be substantial and result in over three order of magnitude differences in LC50 values among clones of a single species. This body of work provides an excellent example of the importance of genotype x environment interaction (see especially Figs. 2 and 4 in chapter 11) and highlights the challenges we face in trying to extrapolate ecotoxicologicai responses across genotypes and/or toxicants.

What Roles Does Genetics have to Play in Ecological Risk Assessment?

Shugart’s contribution (chapter 8) describes how specific types of damage to the structure of DNA can provide valuable endpoints of toxicant exposure. The usefulness of such molecular biomarkers for ecological risk assessment has been questioned on the grounds that DNA damage may not be coupled to ecological effects. As Shugart notes, the relevance of genetic damage for predicting effects at population and higher levels is problematic. However, as indicators of exposure, changes in DNA can be quite powerful tools that, in combination with independently derived ecological effect levels, can play an important part in the risk assessment process. Advantages of DNA markers as indicators of exposure over traditional measures of environmental exposure concentrations include the fact that toxicant bioavailability is accounted for, the techniques are sensitive, and they do not necessarily require that monitoring organisms be destroyed.

Tests of survival and reproduction in the water flea, Daphnia magna, provide key endpoints for ecological effects assessment and are among the few ecotoxicological tests that provide the basis for legislative decisions. Present internationally agreed test protocols (OECD 1997) are confined to examining survival and asexual reproduction in single clones of Daphnia, despite the fact that, in nature, Daphnia reproduces both sexually and asexually, and its populations are made up of a mixture of genotypes. As discussed by Baird and Barata (chapter 11) and Forbes et al. (chapter 10) partheno-genetically reproducing clones offer several advantages, the most important of which is that they may facilitate identification and quantification of the role of genetic factors in controlling responses to toxicants. However, the experiments of Snell et al. (chapter 9 and references therein), using another cyclical parthenogen, indicate that there may be significant differences in the exposure concentrations at which sexual and asexual reproduction become impaired. If the pattern found by Snell et al. turns out to apply to other cyclical parthenogens such as Daphnia, then confining test protocols to the asexual phase of the life-cycle of test populations is likely to underestimate toxicant risks to natural populations. Despite their obvious convenience, parthenogentically reproducing organisms may turn out to be a bad choice for ecotoxicological effects assessment.

If, as Baird and Barata (chapter 11) suggest, the degree of genetic variation in organism response to toxicant exposure is substance and species specific, how can we deal with this uncertainty in ecotoxicological risk assessment? As one possibility, Baird and Barata suggest that the distribution of sensitivities of genotypes in selected populations be examined. The distribution of genotype sensitivities could be used to estimate species protection criteria in the same way that species sensitivity distributions have been extrapolated to derive ecosystem protection criteria (Stephan et al. 1985; Wagner and Lokke 1991; Aldenberg and Slob 1993). The extrapolation models applied at the species-to-ecosystem level suffer from a number of weaknesses (Forbes and Forbes 1994). Among them are that the species used to fit the sensitivity distributions are neither a random sample of species nor necessarily even members of the ecosystem(s) for which extrapolations are being made. Fitting a sensitivity distribution at the genotype-to-population level could at least avoid these two potentially important pitfalls and may help to better quantify the extent to which uncertainty due to genetic influences needs to be incorporated into risk estimates.

Another approach for incorporating genetic uncertainty (also discussed by Baird and Barata, chapter 11) could be to use the observed clone-to-clone differences as an argument for maintaining or even increasing the application factors for prediction of no-effect concentrations from test data. In this regard, it is tempting to conclude that if different genotypes of a single population vary substantially from each other in their responses to toxicant exposure, such variability will be magnified if we compare different populations and species. However, the results presented by Forbes et al. (chapter 10) challenge this assumption. They found that geographically distinct populations of Artemia species responded similarly to copper exposure whereas the major source of variability was among individuals within single clones.

Quantifying uncertainty in susceptibility to toxicants is an important aspect of both ecological and human health risk assessment, and genetic factors can be an important source of this uncertainty. There is a pressing need for better models that can account for genetic differences in susceptibility to toxicant exposure and can incorporate this uncertainty into risk estimates.

Challenges for the Future

Although there are good reasons to believe that adaptation of organisms to toxicants involves certain costs (Forbes and Calow 1996; Theodorakis and Shugart chapter 7), identifying and quantifying these costs remain a challenge. Shaw (chapter 2) discusses the diff...