Abstract
Quantitative genetic approaches are often used to study evolutionary processes in ecotoxicology. This paper focuses on the evolution of resistance to environmental contaminants—an important evolutionary process in ecotoxicology. Three approaches are commonly employed to study the evolution of resistance: (1) Assessing whether a contaminant-exposed population has an increased resistance relative to a control population, using either spatial or temporal comparisons. (2) Estimating a population’s heritability of resistance. (3) Investigating responses in a laboratory selection experiment. All three approaches provide valuable information on the potential for contaminants to affect a population’s evolutionary trajectory via natural selection. However, all three approaches have inherent limitations, including difficulty in separating the various genetic and environmental variance components, responses being dependent on specific population and testing conditions, and inability to fully capture natural conditions in the laboratory. In order to maximize insights into the long-term consequences of adaptation, it is important to not just look at resistance itself, but also at the fitness consequences and at correlated responses in characteristics other than resistance. The rapid development of molecular genetics has yielded alternatives to the “black box” approach of quantitative genetics, but the presence of different limitations and strengths in the two fields means that they should be viewed as complementary rather than exchangeable. Quantitative genetics is benefiting from the incorporation of molecular tools and remains an important field for studying evolutionary toxicology.
Similar content being viewed by others
References
Agrawal AA, Stinchcombe JR (2009) How much do genetic covariances alter the rate of adaptation? Proc R Soc B 276:1183–1191
Andrew RL, Peakall R, Wallis IR, Wood JT, Knight EJ, Foley WJ (2005) Marker-based quantitative genetics in the wild? The heritability and genetic correlation of chemical defenses in Eucalyptus. Genetics 171:1989–1998
Antonovics J, Bradshaw AD, Turner RG (1971) Heavy metal tolerance in plants. Adv Ecol Res 7:1–85
Arnaud L, Haubruge E (2002) Insecticide resistance enhances male reproductive success in a beetle. Evolution 56:2435–2444
Arnold SJ (1994) Multivariate inheritance and evolution: a review of concepts. In: Boake CRB (ed) Quantitative genetic studies of behavioral evolution. University of Chicago Press, Chicago, IL, pp 17–48
Athrey NRG, Leberg PL, Klerks PL (2007) Laboratory culturing and selection for increased resistance to cadmium reduce genetic variation in the least killifish, Heterandria formosa. Environ Toxicol Chem 26:1916–1921
Barata C, Baird DJ, Mitchell SE, Soares AMVM (2002) Among- and within-population variability in tolerance to cadmium stress in natural populations of Daphnia magna: Implications for ecological risk assessment. Environ Toxicol Chem 21:1058–1064
Bhave MR, Wilson MJ, Waalkes MP (1988) Methylation status and organization of the metallothionein-Ι gene in livers and testes of strains of mice resistant and susceptible to cadmium. Toxicology 50:231–245
Boyd CE, Ferguson DE (1964) Susceptibility and resistance of mosquito fish to several insecticides. J Econ Entomol 57:430–431
Brown BE (1978) Lead detoxification by a copper-tolerant isopod. Nature 276:388–390
Bryan GW, Hummerstone LG (1971) Adaptation of the polychaete Nereis diversicolor to sediments containing high concentrations of heavy metals. I. General observations and adaptation to copper. J Mar Biol Assoc 51:845–863
Bubliy OA, Loeschcke V (2002) Effect of low stressful temperature on genetic variation of five quantitative traits in Drosophila melonagaster. Heredity 89:70–75
Carvajal-Rodríguez A, Rolán-Alvarez E, Caballero A (2005) Quantitative variation as a tool for detecting human-induced impacts on genetic diversity. Biol Conserv 124:1–13
Charmantier A, Garant D (2005) Environmental quality and evolutionary potential: lessons from wild populations. Proc R Soc B 272:1415–1425
Chaumot A, Gos P, Garric J, Geffard O (2009) Additive vs non-additive genetic components in lethal cadmium tolerance of Gammarus (Crustacea): novel light on the assessment of the potential for adaptation to contamination. Aquat Toxicol 94:294–299
Chown SL, Jumbam KR, Sørensen JG, Terblanche JS (2009) Phenotypic variance, plasticity and heritability estimates of critical thermal limits depend on methodological context. Funct Ecol 23:133–140
Crow JF (1957) Genetics of insect resistance to chemicals. Ann Rev Entomol 2:227–246
Damásio J, Guilhermino L, Soares AMVM, Riva MC, Barata C (2007) Biochemical mechanisms of resistance in Daphnia magna exposed to the insecticide fenitrothion. Chemosphere 70:74–82
Derry AM, Arnott SE, Boag PT (2010) Evolutionary shifts in copepod acid tolerance in an acid-recovering lake indicated by resurrected resting eggs. Evolut Ecol 24:133–145
Donker MH, Bogert CG (1991) Adaptation to cadmium in three populations of the isopod Porcellio scaber. Comp Biochem Physiol 100C:143–146
Donker MH, Koevoets P, Verkleij JAC, Van Straalen NM (1990) Metal binding compounds in the hepatopancreas and haemolymph of Porcellio scaber (Isopoda) from contaminated and reference areas. Comp Biochem Physiol 97C:119–126
Eränen JK, Nilsen J, Zverev VE, Kozlov MV (2009) Mountain birch under multiple stressors—heavy metal-resistant populations co-resistant to biotic stress but maladapted to abiotic stress. J Evol Biol 22:840–851
Falconer DS (1960) Introduction to quantitative genetics, 1st edn. Oliver & Boyd, Edinburgh
Falconer DS, Mackay TFC (1996) Introduction to quantitative genetics, 4th edn. Longman, Essex
Firko MJ, Hayes JL (1990) Quantitative genetic tools for insecticide resistance risk assessment: estimating the heritability of resistance. J Econ Entomol 83:647–654
Fuller RC, Baer CF, Travis J (2005) How and when selection experiments might actually be useful. Integr Comp Biol 45:391–404
Garant D, Kruuk LEB (2005) How to use molecular marker data to measure evolutionary parameters in wild populations. Mol Ecol 14:1843–1859
Garant D, Hadfield JD, Kruuk LEB, Sheldon BC (2008) Stability of genetic variance and covariance for reproductive characters in the face of climate change in a wild bird population. Mol Ecol 17:179–188
Georghiou GP (1990) Overview of insecticide resistance. In: Green MB, LeBaron HM, Moberg WK (eds) Managing resistance to agrochemicals. American Chemical Society, Washington, DC, pp 18–41
Hoffmann AA, Willi Y (2008) Detecting genetic responses to environmental change. Nat Rev Genet 9:421–432
Hoffmann AA, Sørensen JG, Loeschcke V (2003) Adaptation of Drosophila to temperature extremes: bringing together quantitative and molecular approaches. J Thermal Biol 28:175–216
Houle D (1991) Genetic covariance of fitness correlates: what genetic correlations are made of and why it matters. Evolution 45:630–648
Houle D (1992) Comparing evolvability and variability of quantitative traits. Genetics 130:195–204
Jiménez-Ambriz G, Petit C, Bourrié I, Dubois S, Olivieri I, Ronce O (2007) Life history variation in the heavy metal tolerant plant Thlaspi caerulescens growing in a network of contaminated and noncontaminated sites in southern France: role of gene flow, selection, and phenotypic plasticity. New Phytol 173:199–215
Johnson MTJ, Agrawal AA, Maron JL, Salminen J-P (2009) Heritability, covariation and natural selection on 24 traits of common evening primrose (Oenothera biennis) from a field experiment. J Evol Biol 22:1295–1307
Klerks PL, Bartholomew PR (1991) Cadmium accumulation and detoxification in a Cd-resistant population of the oligochaete Limnodrilus hoffmeisteri. Aquat Toxicol 19:97–112
Klerks PL, Lentz SA (1998) Resistance to lead and zinc in the western mosquitofish Gambusia affinis inhabiting contaminated Bayou Trepagnier. Ecotoxicology 7:11–17
Klerks PL, Levinton JS (1989) Rapid evolution of metal resistance in a benthic oligochaete inhabiting a metal-polluted site. Biol Bull 176:135–141
Klerks PL, Levinton JS (1993) Evolution of resistance and changes in community composition in metal-polluted environments: a case study on Foundry Cove. In: Dallinger R, Rainbow PS (eds) Ecotoxicology of metals in invertebrates. CRC Press, Boca Raton, FL, pp 223–241
Klerks PL, Moreau CJ (2001) Heritability of resistance to individual contaminants and to contaminant mixtures in the sheepshead minnow (Cyprinodon variegatus). Environ Toxicol Chem 20:1746–1751
Klerks PL, Weis JS (1987) Genetic adaptation to heavy metals in aquatic organisms: a review. Environ Pollut 45:173–205
Knutson AB, Klerks PL, Levinton JS (1987) The fate of metal contaminated sediments in Foundry Cove, New York. Environ Pollut 45:291–304
Lande R, Arnold SJ (1983) The measurement of selection on correlated characters. Evolution 37:1210–1226
LeBlanc GA (1982) Laboratory investigation into the development of resistance of Daphnia magna (Straus) to environmental pollutants. Environ Pollut (Ser A) 27:309–322
Leinonen T, O’Hara RB, Cano JM, Merilä J (2008) Comparative studies of quantitative trait and neutral marker divergence: a meta-analysis. J Evol Biol 21:1–17
Levinton JS, Suatoni E, Wallace W, Junkins R, Kelaher B, Allen BJ (2003) Rapid loss of genetically based resistance to metals after the clean-up of a Superfund site. Proc Natl Acad Sci USA 100:9889–9891
Lonsdale DJ, Levinton JS (1985) Latitudinal differentiation in embryonic duration, egg size, and newborn survival in a harpacticoid copepod. Biol Bull 168:419–431
Lopes I, Baird DJ, Ribeiro R (2005) Genetically determined resistance to lethal levels of copper by Daphnia longispina: association with sublethal response and multiple/coresistance. Environ Toxicol Chem 24:1414–1419
Mackie JA, Levinton JS, Przeslawski R, DeLambert D, Wallace W (2010) Loss of evolutionary resistance by the oligochaete Limnodrilus hoffmeisteri to a toxic substance—cost or gene flow? Evolution 64:152–165
Macnair MR (1991) Why the evolution of resistance to anthropogenic toxins normally involves major gene changes: the limits to natural selection. Genetica 84:213–219
Macnair MR (1997) The evolution of plants in metal-contaminated environments. In: Bijlsma R, Loeschcke V (eds) Environmental stress, adaptation and evolution. Birkhäuser Verlag, Basel, pp 3–24
Maroni G, Wise J, Young JE, Otto R (1987) Metallothionein gene duplication and metal tolerance in natural populations of Drosophila melanogaster. Genetics 117:739–744
Martínez DE, Levinton J (1996) Adaptation to heavy metals in the aquatic oligochaete Limnodrilus hoffmeisteri: evidence for control by one gene. Evolution 50:1339–1343
McGuigan K, Blows MW (2010) Evolvability of individual traits in a multivariate context: partitioning the additive genetic variance into common and specific components. Evolution 64:1899–1911
Meyer JN, Wassenberg DM, Karchner SI, Hahn ME, Di Giulio RT (2003) Expression and inducibility of aryl hydrocarbon receptor pathway genes in wild-caught killifish (Fundulus heteroclitus) with different contaminant-exposure histories. Environ Toxicol Chem 22:2337–2343
Meyer J, Volz DC, Freedman JH, Di Giulio RT (2005) Differential display of hepatic mRNA from killifish (Fundulus heteroclitus) inhabiting a Superfund estuary. Aquat Toxicol 73:327–341
Ownby DR, Newman MC, Mulvey M, Vogelbein WK, Unger MA, Arzayus LF (2002) Fish (Fundulus heteroclitus) populations with different exposure histories differ in tolerance of creosote-contaminated sediments. Environ Toxicol Chem 21:1897–1902
Posthuma L (1990) Genetic differentiation between populations of Orchesella cincta (Collembola) from heavy metal contaminated sites. J Appl Ecol 27:609–622
Posthuma L, Hogervorst RF, Van Straalen NM (1992) Adaptation to soil pollution by cadmium excretion in natural populations of Orchesella cincta (L.) (Collembola). Arch Environ Contam Toxicol 22:146–156
Posthuma L, Hogervorst RF, Joosse ENG, Van Straalen NM (1993) Genetic variation and covariation for characteristics associated with cadmium tolerance in natural populations of the springtail Orchesella cincta (L.). Evolution 47:619–631
Powell WH, Bright R, Bello SM, Hahn ME (2000) Developmental and tissue-specific expression of AHR1, AHR2, and ARNT2 in dioxin-sensitive and -resistant populations of the marine fish Fundulus heteroclitus. Toxicol Sci 57:229–239
Rahel F (1981) Selection for zinc tolerance in fish: results from laboratory and wild populations. Trans Am Fish Soc 110:19–28
Roelofs D, Overhein L, De Boer ME, Janssens TKS, Van Straalen NM (2006) Additive genetic variation of transcriptional regulation: metallothionein expression in the soil insect Orchesella cincta. Heredity 96:85–92
Roff DA (1997) Evolutionary quantitative genetics. Chapman & Hall, New York
Routtu J, Jansen B, Colson I, De Meester L, Ebert D (2010) The first-generation Daphnia magna linkage map. BMC Genomics 11:508
Scott JA, Plapp FW Jr, Bay DE (1997) Pyrethroid resistance associated with decreased biotic fitness in horn flies (Diptera: Muscidae). Southw Entomol 122:405–410
Shirley MDF, Sibly RM (1999) Genetic basis of a between-environment trade-off involving resistance to cadmium in Drosophila melanogaster. Evolution 53:826–836
Svetec N, Werzner A, Wilches R, Pavlidis P, Broman KW, Metzler D, Stephan W (2011) Identification of X-linked quantitative trait loci affecting cold tolerance in Drosophila melanogaster and fine mapping with selective sweep analysis. Mol Ecol 20:530–544
Van Noordwijk AJ, Van Balen JH, Scharloo W (1980) Heritability of ecologically important traits in the great tit. Ardea 68:193–203
Vinson SB, Boyd CE, Ferguson DE (1963) Resistance to DDT in the mosquito fish, Gambusia affinis. Science 139:217–218
Wallace WW, Lopez GR, Levinton JS (1998) Cadmium resistance in an oligochaete and its effect on cadmium trophic transfer to an omnivorous shrimp. Mar Ecol Prog Ser 172:225–237
Ward TJ, Robinson WE (2005) Evolution of cadmium resistance in Daphnia magna. Environ Toxicol Chem 24:2341–2349
Weider LJ, Lampert W, Wessels M, Colbourne JK, Limburg P (1997) Long-term genetic shifts in a microcrustacean egg bank associated with anthropogenic changes in the Lake Constance ecosystem. Proc R Soc B 264:1613–1618
Weigensberg I, Roff DA (1996) Natural heritabilities: can they be reliably estimated in the laboratory? Evolution 50:2149–2157
Wilson AJ (2008) Why h 2 does not always equal V A /V P . J Evol Biol 21:647–650
Wirgin I, Roy NK, Loftus M, Chambers RC, Franks DG, Hahn ME (2011) Mechanistic basis of resistance to PCBs in atlantic tomcod from the Hudson River. Sciencexpress. doi:10.1126/science.1197296
Xie L, Klerks PL (2003) Responses to selection for cadmium resistance in the least killifish, Heterandria formosa. Environ Toxicol Chem 22:313–320
Xie L, Klerks PL (2004) Fitness costs of resistance to cadmium in the least killifish (Heterandria formosa). Environ Toxicol Chem 23:1499–1503
Acknowledgment
We thank Carlos Barata and Marie-Agnes Coutellec for organizing this special issue and for their insightful and helpful comments on an earlier version of this manuscript.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Klerks, P.L., Xie, L. & Levinton, J.S. Quantitative genetics approaches to study evolutionary processes in ecotoxicology; a perspective from research on the evolution of resistance. Ecotoxicology 20, 513–523 (2011). https://doi.org/10.1007/s10646-011-0640-2
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10646-011-0640-2