Evolutionary Genomics of Environmental Pollution

  • Andrew WhiteheadEmail author
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 781)


Chemical toxins have been a persistent source of evolutionary challenges throughout the history of life, and deep within the genomic storehouse of evolutionary history lay ancient adaptations to diverse chemical poisons. However, the rate of change of contemporary environments mediated by human-introduced pollutants is rapidly screening this storehouse and severely testing the adaptive potential of many species. In this chapter, we briefly review the deep history of evolutionary adaptation to environmental toxins, and then proceed to describe the attributes of stressors and populations that may facilitate contemporary adaptation to pollutants introduced by humans. We highlight that phenotypes derived to enable persistence in polluted habitats may be multi-dimensional, requiring global genome-scale tools and approaches to uncover their mechanistic basis, and include examples of recent progress in the field. The modern tools of genomics offer promise for discovering how pollutants interact with genomes on physiological timescales, and also for discovering what genomic attributes of populations may enable resistance to pollutants over evolutionary timescales. Through integration of these sophisticated genomics tools and approaches with an understanding of the deep historical forces that shaped current populations, a more mature understanding of the mechanistic basis of contemporary ecological-evolutionary dynamics should emerge.


Contemporary evolution Evolutionary-ecological dynamics Evolutionary genomics Ecological genomics Comparative genomics Toxicogenomics Pollution Adaptation Evolutionary toxicology 




The aryl hydrocarbon receptor (AHR) is a cytosolic transcription factor. Pollutants such as dioxins, PCBs, and PAHs, act as ligands for this receptor. Once activated, the receptor-ligand complex migrates to the nucleus, and acts as a transcription factor to activate the transcription of a battery of genes. Some of the activated genes are responsible for metabolism of the ligand and for the emergence of toxicity


Anthropogenic refers to effects or objects that are of human origin, or that are influenced by humans

Comparative transcriptomics

Comparative transcriptomics is an experimental design that includes the comparison of transcriptomic responses to some experimental variable (e.g., environmental or pollutant challenge) between strains, populations, or species


A contaminant is a compound that is released into the environment as a result of human activities, but that may or may not be toxic to exposed organisms

Contemporary evolution

Contemporary evolution refers to evolutionary change in response to recent changes in the environment

Copy number variation

Specific regions of the genome may increase in copy number from duplication of chromosome segments, duplication of whole chromosomes, or duplication of entire genomes. Protein family expansion (e.g., globins, HOX genes) is often from duplication of chromosome segments that include an entire protein sequence. The fate of duplicate copies may include pseudogenization, maintenance of function, neofunctionalization, or subfunctionalization


Epistasis is a phenomenon that refers to the non-additive effects of multiple genes, where the effects of different loci are not independent – where the effects of one gene are dependent on other genes

Genome scan

Given genome-scale sequence data for many individuals for two or more populations, genome scans are a suite of exploratory methods that are designed to detect genetic signatures of natural selection in populations. Genetic markers that exhibit signatures of selection could be the causative genetic variants, but are more likely to be physically linked to causative variants


Neofunctionalization is a result of functional divergence of gene paralogs following duplication, where the duplicate copy acquires an entirely new function that is distinct from the original gene’s functions


Polycyclic aromatic hydrocarbons (PAHs) are a class of chemicals that are common environmental pollutants, where major sources are from spilled crude oil and from fuel combustion. PAHs act as ligands for the AHR, and exert at least part of their toxicity through the activation of the AHR signaling pathway


Polychlorinated biphenyls (PCBs) are a class of chemicals that are persistent environmental pollutants, where major sources are from wastes from industrial processes where they were used as coolant fluids, hydraulic fluids, and insulation fluids. PCBs act as ligands for the AHR, and exert at least part of their toxicity through the activation of the AHR signaling pathway


A gene product is considered pleiotropic if it influences more than one phenotypic trait


A pollutant is a compound that is released into the environment as a result of human activities, and that has negative effects in exposed organisms

QTL mapping

Quantitative trait locus (QTL) mapping involves matching genotype to phenotype from experimental crosses to detect genetic variants that are physically linked to phenotypes of interest. Genetic markers that are associated with the phenotype are not necessarily the causative loci, but are presumed to be physically linked with causative loci


Subfunctionalization is a result of functional divergence of gene paralogs following duplication, where the duplicate copies retain different parts of the original gene’s functions


Toxicants are chemicals that exert toxic effects at sufficiently high doses, and that are not natural products, but rather products of human activity


Toxins are chemicals that exert toxic effects at sufficiently high doses, and that are natural products of biosynthesis by organisms.


A compound that may be found within organisms, but that is foreign to those organisms, usually in reference to manufactured chemicals


  1. Agra AR, Guilhermino L, Soares AMVM, Barata C (2010) Genetic costs of tolerance to metals in Daphnia longispina populations historically exposed to a copper mine drainage. Environ Toxicol Chem 29:939–946PubMedGoogle Scholar
  2. Allendorf FW, Hard JJ (2009) Human-induced evolution caused by unnatural selection through harvest of wild animals. Proc Natl Acad Sci USA 106:9987–9994PubMedGoogle Scholar
  3. Antonovics J, Bradshaw AD, Turner RG (1971) Heavy metal tolerance in plants. Adv Ecol Res 7:1–85Google Scholar
  4. Barbaro G, Scozzafava A, Mastrolorenzo A, Supuran CT (2005) Highly active antiretroviral therapy: current state of the art, new agents and their pharmacological interactions useful for improving therapeutic outcome. Curr Pharm Design 11:1805–1843Google Scholar
  5. Becher M, Talke IN, Krall L, Kramer U (2004) Cross-species microarray transcript profiling reveals high constitutive expression of metal homeostasis genes in shoots of the zinc hyperaccumulator Arabidopsis halleri. Plant J 37:251–268PubMedGoogle Scholar
  6. Beckie HJ, Reboud X (2009) Selecting for weed resistance: herbicide rotation and mixture. Weed Technol 23:363–370Google Scholar
  7. Bello SM, Franks DG, Stegeman JJ, Hahn ME (2001) Acquired resistance to aryl hydrocarbon receptor agonists in a population of Fundulus heteroclitus from a marine superfund site: in vivo and in vitro studies on the induction of xenobiotic-metabolizing enzymes. Toxicol Sci 60:77–91PubMedGoogle Scholar
  8. Bernhardt R (2006) Cytochromes P450 as versatile biocatalysts. J Biotechnol 124:128–145PubMedGoogle Scholar
  9. Blaustein AR, Belden LK (2003) Amphibian defenses against ultraviolet-B radiation. Evol Dev 5:89–97PubMedGoogle Scholar
  10. Bozinovic G, Oleksiak MF (2010) Embryonic gene expression among pollutant resistant and sensitive Fundulus heteroclitus populations. Aquat Toxicol 98:221–229PubMedGoogle Scholar
  11. Campbell BJ, Smith JL, Hanson TE, Klotz MG, Stein LY, Lee CK, Wu DY, Robinson JM, Khouri HM, Eisen JA, Cary SC (2009) Adaptations to submarine hydrothermal environments exemplified by the genome of Nautilia profundicola. Plos Genet 5(2):e1000362Google Scholar
  12. Chevin LM, Lande R, Mace GM (2010) Adaptation, plasticity, and extinction in a changing environment: towards a predictive theory. Plos Biol 8(4):e1000357Google Scholar
  13. Clark BW, Di Giulio RT (2012) Fundulus heteroclitus adapted to PAHs are cross-resistant to multiple insecticides. Ecotoxicology 21:465–474PubMedGoogle Scholar
  14. Clark BW, Matson CW, Jung D, Di Giulio RT (2010) AHR2 mediates cardiac teratogenesis of polycyclic aromatic hydrocarbons and PCB-126 in Atlantic killifish (Fundulus heteroclitus). Aquat Toxicol 99:232–240PubMedGoogle Scholar
  15. Cohen S (2002) Strong positive selection and habitat-specific amino acid substitution patterns in MHC from an estuarine fish under intense pollution stress. Mol Biol Evol 19:1870–1880PubMedGoogle Scholar
  16. Colosimo PF, Hosemann KE, Balabhadra S, Villarreal G, Dickson M, Grimwood J, Schmutz J, Myers RM, Schluter D, Kingsley DM (2005) Widespread parallel evolution in sticklebacks by repeated fixation of ectodysplasin alleles. Science 307:1928–1933PubMedGoogle Scholar
  17. Cook LM, Grant BS, Saccheri IJ, Mallet J (2012) Selective bird predation on the peppered moth: the last experiment of Michael Majerus. Biol Lett 8:609–612PubMedGoogle Scholar
  18. Coyle P, Philcox JC, Carey LC, Rofe AM (2002) Metallothionein: the multipurpose protein. Cell Mol Life Sci 59:627–647PubMedGoogle Scholar
  19. Dawkins R (1983) The extended phenotype: the long reach of the gene. Oxford University Press, OxfordGoogle Scholar
  20. D’Costa VM, King CE, Kalan L, Morar M, Sung WWL, Schwarz C, Froese D, Zazula G, Calmels F, Debruyne R, Golding GB, Poinar HN, Wright GD (2011) Antibiotic resistance is ancient. Nature 477:457–461PubMedGoogle Scholar
  21. De Schamphelaere KA, Glaholt S, Asselman J, Messiaen M, De Coninck D, Janssen CR, Colbourne JK, Shaw JR (2011) Will genetic adaptation of natural populations to chemical pollution result in lower or higher tolerance to future climate change? Integr Environ Assess Manag 7:141–143PubMedGoogle Scholar
  22. Despres L, David JP, Gallet C (2007) The evolutionary ecology of insect resistance to plant chemicals. Trends Ecol Evol 22:298–307PubMedGoogle Scholar
  23. Elskus AA, Monosson E, McElroy AE, Stegeman JJ, Woltering DS (1999) Altered CYP1A expression in Fundulus heteroclitus adults and larvae: a sign of pollutant resistance? Aquat Toxicol 45:99–113Google Scholar
  24. Feyereisen R (1999) Insect P450 enzymes. Annu Rev Entomol 44:507–533PubMedGoogle Scholar
  25. Ffrench-Constant RH, Daborn PJ, Le Goff G (2004) The genetics and genomics of insecticide resistance. Trends Genet 20:163–170PubMedGoogle Scholar
  26. Geffeney SL, Fujimoto E, Brodie ED, Brodie ED, Ruben PC (2005) Evolutionary diversification of TTX-resistant sodium channels in a predator–prey interaction. Nature 434:759–763PubMedGoogle Scholar
  27. Ghosh R, Andersen EC, Shapiro JA, Gerke JP, Kruglyak L (2012) Natural variation in a chloride channel subunit confers avermectin resistance in C. elegans. Science 335:574–578PubMedGoogle Scholar
  28. Gluckman PD, Beedle A, Hanson MA (2009) Principles of evolutionary medicine. Oxford University Press, OxfordGoogle Scholar
  29. Goldstone JV, Goldstone HMH, Morrison AM, Tarrant A, Kern SE, Woodin BR, Stegeman JJ (2007) Cytochrome p450 1 genes in early deuterostomes (tunicates and sea urchins) and vertebrates (chicken and frog): origin and diversification of the CYP1 gene family. Mol Biol Evol 24:2619–2631PubMedGoogle Scholar
  30. Gonzalez FJ, Nebert DW (1990) Evolution of the P450-gene superfamily – animal plant warfare, molecular drive and human genetic-differences in drug oxidation. Trends Genet 6:182–186PubMedGoogle Scholar
  31. Graur D, Li W-H (2000) Fundamentals of molecular evolution. Sinauer Associates, SunderlandGoogle Scholar
  32. Hahn ME, Karchner SI, Franks DG, Merson RR (2004) Aryl hydrocarbon receptor polymorphisms and dioxin resistance in Atlantic killifish (Fundulus heteroclitus). Pharmacogenetics 14:131–143PubMedGoogle Scholar
  33. Hahn ME, Karchner SI, Franks DG, Evans BR, Nacci D, Champlin D, Cohen S (2005) Mechanism of PCB – and dioxin-resistance in fish in the Hudson River Estuary: role of receptor polymorphisms. Final report, Hudson River Foundation Grant 004/02AGoogle Scholar
  34. Hairston NG, Ellner SP, Geber MA, Yoshida T, Fox JA (2005) Rapid evolution and the convergence of ecological and evolutionary time. Ecol Lett 8:1114–1127Google Scholar
  35. Hanikenne M, Talke IN, Haydon MJ, Lanz C, Nolte A, Motte P, Kroymann J, Weigel D, Kramer U (2008) Evolution of metal hyperaccumulation required cis-regulatory changes and triplication of HMA4. Nature 453:391–395, U344PubMedGoogle Scholar
  36. Harbeitner RC, Hahn ME, Timme-Laragy AR (2013) Differential sensitivity to pro-oxidant exposure in two populations of killifish (Fundulus heteroclitus). Ecotoxicology 22:387–401PubMedGoogle Scholar
  37. Hartley CJ, Newcomb RD, Russell RJ, Yong CG, Stevens JR, Yeates DK, La Salle J, Oakeshott JG (2006) Amplification of DNA from preserved specimens shows blowflies were preadapted for the rapid evolution of insecticide resistance. Proc Natl Acad Sci USA 103:8757–8762PubMedGoogle Scholar
  38. Hendry AP, Kinnison MT (1999) Perspective: the pace of modern life: measuring rates of contemporary microevolution. Evolution 53:1637–1653Google Scholar
  39. Hendry AP, Farrugia TJ, Kinnison MT (2008) Human influences on rates of phenotypic change in wild animal populations. Mol Ecol 17:20–29PubMedGoogle Scholar
  40. Hendry AP, Kinnison MT, Heino M, Day T, Smith TB, Fitt G, Bergstrom CT, Oakeshott J, Jorgensen PS, Zalucki MP, Gilchrist G, Southerton S, Sih A, Strauss S, Denison RF, Carroll SP (2011) Evolutionary principles and their practical application. Evol Appl 4:159–183Google Scholar
  41. Hoffmann AA, Sgro CM (2011) Climate change and evolutionary adaptation. Nature 470:479–485PubMedGoogle Scholar
  42. Hohenlohe PA, Bassham S, Etter PD, Stiffler N, Johnson EA, Cresko WA (2010) Population genomics of parallel adaptation in threespine stickleback using sequenced RAD tags. Plos Genet 6(2):e1000862Google Scholar
  43. Jansen M, Coors A, Stoks R, De Meester L (2011) Evolutionary ecotoxicology of pesticide resistance: a case study in Daphnia. Ecotoxicology 20:543–551PubMedGoogle Scholar
  44. Kettlewell B (1973) The evolution of melanism. The study of a recurring necessity; with special reference to industrial melanism in the Lepidoptera. Clarendon, OxfordGoogle Scholar
  45. Kikuchi Y, Hayatsu M, Hosokawa T, Nagayama A, Tago K, Fukatsu T (2012) Symbiont-mediated insecticide resistance. Proc Natl Acad Sci USA 109:8618–8622PubMedGoogle Scholar
  46. King RB (2003) Mendelian inheritance of melanism in the garter snake Thamnophis sirtalis. Herpetologica 59:484–489Google Scholar
  47. Kinnison MT, Hendry AP (2001) The pace of modern life II: from rates of contemporary microevolution to pattern and process. Genetica 112:145–164PubMedGoogle Scholar
  48. Kiontke S, Geisselbrecht Y, Pokorny R, Carell T, Batschauer A, Essen LO (2011) Crystal structures of an archaeal class II DNA photolyase and its complex with UV-damaged duplex DNA. Embo J 30:4437–4449PubMedGoogle Scholar
  49. Klerks PL, Bartholomew PR (1991) Cadmium accumulation and detoxification in a Cd-resistant population of the oligochaete Limnodrilus-hoffmeisteri. Aquat Toxicol 19:97–112Google Scholar
  50. Klerks PL, Levinton JS (1989) Rapid evolution of metal resistance in a benthic oligochaete inhabiting a metal-polluted site. Biol Bull 176:135–141Google Scholar
  51. Klerks PL, Weis JS (1987) Genetic adaptation to heavy-metals in aquatic organisms – a review. Environ Pollut 45:173–205PubMedGoogle Scholar
  52. Klerks PL, Xie LT, Levinton JS (2011) Quantitative genetics approaches to study evolutionary processes in ecotoxicology; a perspective from research on the evolution of resistance. Ecotoxicology 20:513–523PubMedGoogle Scholar
  53. Kump LR (2008) The rise of atmospheric oxygen. Nature 451:277–278PubMedGoogle Scholar
  54. La Duc MT, Benardini JN, Kempf MJ, Newcombe DA, Lubarsky M, Venkateswaran K (2007) Microbial diversity of Indian Ocean hydrothermal vent plumes: microbes tolerant of desiccation, peroxide exposure, and ultraviolet and gamma-irradiation. Astrobiology 7:416–431PubMedGoogle Scholar
  55. Lacy RC (1987) Loss of genetic diversity from managed populations: interacting effects of drift, mutation, immigration, selection, and population subdivision. Conserv Biol 1:143–158Google Scholar
  56. Laxminarayan R, Heymann DL (2012) Challenges of drug resistance in the developing world. Br Med J 344Google Scholar
  57. Levinton JS, Suatoni E, Wallace W, Junkins R, Kelaher B, Allen BJ (2003) Rapid loss of genetically based resistance to metals after the cleanup of a Superfund site. Proc Natl Acad Sci USA 100:9889–9891PubMedGoogle Scholar
  58. Li XC, Schuler MA, Berenbaum MR (2007) Molecular mechanisms of metabolic resistance to synthetic and natural xenobiotics. Annu Rev Entomol 52:231–253PubMedGoogle Scholar
  59. Lotrich VA (1975) Summer home range and movements of Fundulus heteroclitus (Pisces: Cyprinodontidae) in a tidal creek. Ecology 56:191–198Google Scholar
  60. Lyman WJ (1984) Establishing sediment criteria for chemicals – industrial perspectives. In: Dickson KL, Maki AW, Brungs WA (eds) Fate and effects of sediment-bound chemicals in aquatic systems. Permagon Press, New York, pp 378–387Google Scholar
  61. Macnair MR (1993) The genetics of metal tolerance in vascular plants. New Phytol 124:541–559Google Scholar
  62. Majerus MEN (1998) Melanism: evolution in action. Oxford University Press, OxfordGoogle Scholar
  63. Maron LG, Guimaraes CT, Kirst M, Albert PS, Birchler JA, Bradbury PJ, Buckler ES, Coluccio AE, Danilova TV, Kudrna D, Magalhaes JV, Pineros MA, Schatz MC, Wing RA, Kochian LV (2013) Aluminum tolerance in maize is associated with higher MATE1 gene copy number. Proc Natl Acad Sci USA 110:5241–5246PubMedGoogle Scholar
  64. Maroni G, Wise J, Young JE, Otto E (1987) Metallothionein gene duplications and metal tolerance in natural-populations of Drosophila-melanogaster. Genetics 117:739–744PubMedGoogle Scholar
  65. Marquis O, Miaud C, Ficetola GF, Bocher A, Mouchet F, Guittonneau S, Devaux A (2009) Variation in genotoxic stress tolerance among frog populations exposed to UV and pollutant gradients. Aquat Toxicol 95:152–161PubMedGoogle Scholar
  66. Martinez DE, Levinton J (1996) Adaptation to heavy metals in the aquatic oligochaete Limnodrilus hoffmeisteri: evidence for control by one gene. Evolution 50:1339–1343Google Scholar
  67. Maurice CF, Haiser HJ, Turnbaugh PJ (2013) Xenobiotics shape the physiology and gene expression of the active human gut microbiome. Cell 152:39–50PubMedGoogle Scholar
  68. Mckenzie JA, Batterham P (1994) The genetic, molecular and phenotypic consequences of selection for insecticide resistance. Trends Ecol Evol 9:166–169PubMedGoogle Scholar
  69. McMillan AM, Bagley MJ, Jackson SA, Nacci DE (2006) Genetic diversity and structure of an estuarine fish (Fundulus heteroclitus) indigenous to sites associated with a highly contaminated urban harbor. Ecotoxicology 15:539–548PubMedGoogle Scholar
  70. Medina MH, Correa JA, Barata C (2007) Micro-evolution due to pollution: possible consequences for ecosystem responses to toxic stress. Chemosphere 67:2105–2114PubMedGoogle Scholar
  71. Meyer J, Di Giulio R (2002) Patterns of heritability of decreased EROD activity and resistance to PCB 126-induced teratogenesis in laboratory-reared offspring of killifish (Fundulus heteroclitus) from a creosote-contaminated site in the Elizabeth River, VA, USA. Mar Environ Res 54:621–626PubMedGoogle Scholar
  72. Meyer JN, Di Giulio RT (2003) Heritable adaptation and fitness costs in killifish (Fundulus heteroclitus) inhabiting a polluted estuary. Ecol Appl 13:490–503Google Scholar
  73. Meyer JN, Nacci DE, Di Giulio RT (2002) Cytochrome P4501A (CYP1A) in killifish (Fundulus heteroclitus): heritability of altered expression and relationship to survival in contaminated sediments. Toxicol Sci 68:69–81PubMedGoogle Scholar
  74. Monosson E (2012) Evolution in a toxic world: how life responds to chemical threats. Island Press, Washington, DCGoogle Scholar
  75. Mulvey M, Newman MC, Vogelbein W, Unger MA (2002) Genetic structure of Fundulus heteroclitus from PAH-contaminated and neighboring sites in the Elizabeth and York Rivers. Aquat Toxicol 61:195–209PubMedGoogle Scholar
  76. Mulvey M, Newman MC, Vogelbein WK, Unger MA, Ownby DR (2003) Genetic structure and mtDNA diversity of Fundulus heteroclitus populations from polycyclic aromatic hydrocarbon-contaminated sites. Environ Toxicol Chem 22:671–677PubMedGoogle Scholar
  77. Nacci D, Coiro L, Champlin D, Jayaraman S, McKinney R, Gleason TR, Munns WR, Specker JL, Cooper KR (1999) Adaptations of wild populations of the estuarine fish Fundulus heteroclitus to persistent environmental contaminants. Mar Biol 134:9–17Google Scholar
  78. Nacci DE, Gleason T, Gutjahr-Gobell R, Huber M, Munns WRJ (2002) Effects of environmental stressors on wildlife populations. In: Newman MC (ed) Coastal and Estuarine Risk Assessment: risk on the edge. CRC Press/Lewis Publishers, Washington, DCGoogle Scholar
  79. Nacci D, Champlin D, Jayaraman S (2010) Adaptation of the estuarine fish Fundulus heteroclitus (Atlantic Killifish) to polychlorinated biphenyls (PCBs). Estuar Coast Shelf Sci 33:853–864Google Scholar
  80. Oleksiak MF, Karchner SI, Jenny MJ, Franks DG, Welch DBM, Hahn ME (2011) Transcriptomic assessment of resistance to effects of an aryl hydrocarbon receptor (AHR) agonist in embryos of Atlantic killifish (Fundulus heteroclitus) from a marine Superfund site. BMC Genomics 12:263PubMedGoogle Scholar
  81. Orr HA (2005) The genetic theory of adaptation: a brief history. Nat Rev Genet 6:119–127PubMedGoogle Scholar
  82. Otto E, Young JE, Maroni G (1986) Structure and expression of a tandem duplication of the Drosophila metallothionein gene. Proc Natl Acad Sci USA 83:6025–6029PubMedGoogle Scholar
  83. Ouzounis CA, Kunin V, Darzentas N, Goldovsky L (2006) A minimal estimate for the gene content of the last universal common ancestor – exobiology from a terrestrial perspective. Res Microbiol 157:57–68PubMedGoogle Scholar
  84. 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 21:1897–1902PubMedGoogle Scholar
  85. Palumbi SR (2001) Evolution – humans as the world’s greatest evolutionary force. Science 293:1786–1790PubMedGoogle Scholar
  86. Pelletier F, Garant D, Hendry AP (2009) Eco-evolutionary dynamics. Philos Trans R Soc B 364:1483–1489Google Scholar
  87. Pelz HJ, Rost S, Hunerberg M, Fregin A, Heiberg AC, Baert K, MacNicoll AD, Prescott CV, Walker AS, Oldenburg J, Muller CR (2005) The genetic basis of resistance to anticoagulants in rodents. Genetics 170:1839–1847PubMedGoogle Scholar
  88. Posthuma L, van Straalen NM (1993) Heavy-metal adaptation in terrestrial invertebrates – a review of occurrence, genetics, physiology and ecological consequences. Comp Biochem Phys C 106:11–38Google Scholar
  89. Puinean AM, Foster SP, Oliphant L, Denholm I, Field LM, Millar NS, Williamson MS, Bass C (2010) Amplification of a cytochrome P450 gene is associated with resistance to neonicotinoid insecticides in the aphid Myzus persicae. Plos Genet 6:1–11Google Scholar
  90. Reed RD, Papa R, Martin A, Hines HM, Counterman BA, Pardo-Diaz C, Jiggins CD, Chamberlain NL, Kronforst MR, Chen R, Halder G, Nijhout HF, McMillan WO (2011) Optix drives the repeated convergent evolution of butterfly wing pattern mimicry. Science 333:1137–1141PubMedGoogle Scholar
  91. Roark SA, Nacci D, Coiro L, Champlin D, Guttman SI (2005) Population genetic structure of a nonmigratory estuarine fish (Fundulus heteroclitus) across a strong gradient of polychlorinated biphenyl contamination. Environ Toxicol Chem 24:717–725PubMedGoogle Scholar
  92. Roberts RB, Hu YN, Albertson RC, Kocher TD (2011) Craniofacial divergence and ongoing adaptation via the hedgehog pathway. Proc Natl Acad Sci USA 108:13194–13199PubMedGoogle Scholar
  93. Rockman MV (2012) The QTN program and the alleles that matter for evolution: all that’s gold does not glitter. Evolution 66:1–17PubMedGoogle Scholar
  94. Roelofs D, Janssens TKS, Timmermans MJTN, Nota B, Marien J, Bochdanovits Z, Ylstra B, Van Straalen NM (2009) Adaptive differences in gene expression associated with heavy metal tolerance in the soil arthropod Orchesella cincta. Mol Ecol 18:3227–3239PubMedGoogle Scholar
  95. Roux C, Castric V, Pauwels M, Wright SI, Saumitou-LapradeP, Vekemans X (2011) Does speciation between Arabidopsis halleri and Arabidopsis lyrata coincide with major changes in a molecular target of adaptation? Plos One 6:e26872Google Scholar
  96. Shapiro MD, Marks ME, Peichel CL, Blackman BK, Nereng KS, Jonsson B, Schluter D, Kingsley DM (2004) Genetic and developmental basis of evolutionary pelvic reduction in threespine sticklebacks. Nature 428:717–723PubMedGoogle Scholar
  97. Shine R (2012) Invasive species as drivers of evolutionary change: cane toads in tropical Australia. Evol Appl 5:107–116Google Scholar
  98. Sterenborg I, Roelofs D (2003) Field-selected cadmium tolerance in the springtail Orchesella cincta is correlated with increased metallothionein mRNA expression. Insect Biochem Molec 33:741–747Google Scholar
  99. Sweeney J, Deegan L, Garritt R (1998) Population size and site fidelity of Fundulus heteroclitus in a macrotidal saltmarsh creek. Biol Bull 195:238–239Google Scholar
  100. Teo SLH, Able KW (2003) Habitat use and movement of the mummichog (Fundulus heteroclitus) in a restored salt marsh. Estuar Coast Shelf Sci 26:720–730Google Scholar
  101. van Straalen N, Hoffmann A (2000) Review of experimental evidence for physiological costs of tolerance to toxicants. In: Kammenga J, Laskowski R (eds) Demography in ecotoxicology. Wiley, Chichester, p xix, 297 pGoogle Scholar
  102. Van Veld PA, Nacci DE (2008a) Toxicity resistance. In: Di Giulio RT, Hinton DE (eds) The toxicology of fishes. Taylor and Francis, Boca Raton, pp 597–641Google Scholar
  103. Van Veld PA, Nacci DE (2008b) Toxicity resistance. In: Di Giulio RT, Hinton DE (eds) The toxicology of fishes. Taylor and Francis, Boca RatonGoogle Scholar
  104. van’t Hof AE, Saccheri IJ (2010) Industrial melanism in the peppered moth is not associated with genetic variation in canonical melanisation gene candidates. PLoS One 5:e10889Google Scholar
  105. van’t Hof AE, Edmonds N, Dalikova M, Marec F, Saccheri IJ (2011) Industrial melanism in British peppered moths has a singular and recent mutational origin. Science 332:958–960Google Scholar
  106. Vitousek PM, Mooney HA, Lubchenco J, Melillo JM (1997) Human domination of earth’s ecosystems. Science 277:494–499Google Scholar
  107. Ward TJ, Robinson WE (2005) Evolution of cadmium resistance in Daphnia magna. Environ Toxicol Chem 24:2341–2349PubMedGoogle Scholar
  108. Wen ZM, Rupasinghe S, Niu GD, Berenbaum MR, Schuler MA (2006) CYP6B1 and CYP6B3 of the black swallowtail (Papilio polyxenes): Adaptive evolution through subfunctionalization. Mol Biol Evol 23:2434–2443PubMedGoogle Scholar
  109. Werck-Reichhart D, Feyereisen R (2000) Cytochromes P450: a success story. Genome Biol 1: REVIEWS3003Google Scholar
  110. Whalon ME, Mota-Sanchez D, Hollingworth RM (2008) Global pesticide resistance in arthropods. CABI, WallingfordGoogle Scholar
  111. Whitehead A, Triant DA, Champlin D, Nacci D (2010) Comparative transcriptomics implicates mechanisms of evolved pollution tolerance in a killifish population. Mol Ecol 19:5186–5203PubMedGoogle Scholar
  112. Whitehead A, Pilcher W, Champlin D, Nacci D (2012) Common mechanism underlies repeated evolution of extreme pollution tolerance. Proc R Soc B 279:427–433Google Scholar
  113. Willems G, Drager DB, Courbot M, Gode C, Verbruggen N, Saumitou-Laprade P (2007) The genetic basis of zinc tolerance in the metallophyte Arabidopsis halleri ssp halleri (Brassicaceae): an analysis of quantitative trait loci. Genetics 176:659–674PubMedGoogle Scholar
  114. Williams RJP (2007) A system’s view of the evolution of life. J R Soc Interface 4:1049–1070PubMedGoogle Scholar
  115. Williams LM, Oleksiak MF (2008) Signatures of selection in natural populations adapted to chronic pollution. BMC Evol Biol 8:282PubMedGoogle Scholar
  116. Williams LM, Oleksiak MF (2011) Ecologically and evolutionarily important SNPs identified in natural populations. Mol Biol Evol 28:1817–1826PubMedGoogle Scholar
  117. Williams RJP, Rickaby R (2012) Evolution’s destiny: co-evolving chemistry of the environment and life. Royal Society of Chemistry, LondonGoogle Scholar
  118. Wirgin I, Waldman JR (2004) Resistance to contaminants in North American fish populations. Mutat Res Fundam Mol Mech Mutagenesis 552:73–100Google Scholar
  119. 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. Science 331:1322–1325PubMedGoogle Scholar
  120. Wittkopp PJ, Carroll SB, Kopp A (2003) Evolution in black and white: genetic control of pigment patterns in Drosophila. Trends Genet 19:495–504PubMedGoogle Scholar
  121. Wright GD (2007) The antibiotic resistome: the nexus of chemical and genetic diversity. Nat Rev Microbiol 5:175–186PubMedGoogle Scholar
  122. Yamamoto Y, Stock DW, Jeffery WR (2004) Hedgehog signalling controls eye degeneration in blind cavefish. Nature 431:844–847PubMedGoogle Scholar
  123. Yozzo DJ, Smith DE (1998) Composition and abundance of resident marsh-surface nekton: comparison between tidal freshwater and salt marshes in Virginia, USA. Hydrobiologia 362:9–19Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2014

Authors and Affiliations

  1. 1.Department of Environmental ToxicologyUniversity of CaliforniaDavisUSA

Personalised recommendations