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Adaptation in Polluted Waters: Lessons from Killifish

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Development and Environment

Abstract

The world is changing at a pace that has forced us to reevaluate the capabilities and rate of the evolutionary process. As industrial development continues to increase and as we improve analytical environmental chemistry methods, we have observed a growing number of contaminated environments. This increasing pressure from chronically released and persistent contaminants has amplified the importance of evolutionary toxicology. In this chapter, we aim to convey the principles of this relatively young field through a review of evolutionary adaptation in Atlantic and Gulf killifish (Fundulus heteroclitus and F. grandis). Killifish have been widely studied with regard to evolutionary toxicology and anthropogenic adaptation. In the past 20 years, researchers have identified multiple populations of both F. heteroclitus and F. grandis, which have adapted to resist high levels of various classes of industrial contaminants, including polychlorinated biphenyls (PCBs), polycyclic aromatic hydrocarbons (PAHs), and polychlorinated dibenzo-p-dioxins and furans (PCDD/Fs). Heritability of resistance has been confirmed, with offspring showing a similar capacity to resist the cardiovascular teratogenesis associated with early life stage exposures to dioxin-like compounds (DLCs). As more populations have been discovered and studied, different aspects of the acquired resistance have been revealed, but also unique attributes of the independently adapted populations have been identified. Populations adapted to PAHs exhibit high resistance to many classes of contaminants, while populations adapted to PCB contamination are only partially resistant to PAHs. PAH-adapted populations of F. heteroclitus and PCB-adapted populations of F. grandis are more tolerant to oxidative stress, while PCB-adapted populations of F. heteroclitus are more sensitive. Even geographically close adapted populations in F. grandis differ in their levels of cross-resistance to pesticides. These are only some of the ways in which populations of Fundulus with phenotypically similar genetic adaptations create a much more varied and intricate story to be explored in evolutionary toxicology. Here we summarize considerations in the field of evolutionary toxicology through a case study of anthropogenic adaptation in Fundulus, including its environmental and evolutionary relevance.

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References

  • Adams SM, Lindmeier JB, Duvernell DD (2006) Microsatellite analysis of the phylogeography, Pleistocene history and secondary contact hypotheses for the killifish, Fundulus heteroclitus. Mol Ecol 15:1109–1123

    CAS  PubMed  Google Scholar 

  • Alldredge P, Gutierrez M, Duvernell D, Schaefer J, Brunkow P, Matamoros W (2011) Variability in movement dynamics of topminnow (Fundulus notatus and F. olivaceus) populations. Ecol Freshw Fish 20:513–521

    Google Scholar 

  • Aluru N, Karchner SI, Franks DG, Nacci D, Champlin D, Hahn ME (2015) Targeted mutagenesis of aryl hydrocarbon receptor 2a and 2b genes in Atlantic killifish (Fundulus heteroclitus). Aquat Toxicol 158:192–201

    CAS  PubMed  Google Scholar 

  • Amsterdam A, Nissen RM, Sun ZX, Swindell EC, Farrington S, Hopkins N (2004) Identification of 315 genes essential for early zebrafish development. Proc Natl Acad Sci U S A 101:12792–12797

    CAS  PubMed  PubMed Central  Google Scholar 

  • Anchor QEA (2010) Sediment and surface water contamination of potential concern delineation data report Patrick bayou superfund site, Deer Park

    Google Scholar 

  • Armstrong PB, Child JS (1965) Stages in normal development of Fundulus heteroclitus. Biol Bull 128:143

    Google Scholar 

  • Ashurst SW, Cohen GM, Nesnow S, Digiovanni J, Slaga TJ (1983) Formation of benzo[a]pyrene DNA adducts and their relationship to tumor initiation in mouse epidermis. Cancer Res 43:1024–1029

    CAS  PubMed  Google Scholar 

  • Auld JR, Agrawal AA, Relyea RA (2010) Re-evaluating the costs and limits of adaptive phenotypic plasticity. Proc R Soc B Biol Sci 277:503–511

    Google Scholar 

  • Bacanskas LR, Whitaker J, Di Giulio RT (2004) Oxidative stress in two populations of killifish (Fundulus heteroclitus) with differing contaminant exposure histories. Mar Environ Res 58:597–601

    CAS  PubMed  Google Scholar 

  • Bello SM, Franks DG, Stegeman JJ, Hahn ME (2001) Acquired resistance to Ah receptor agonists in a population of Atlantic killifish (Fundulus heteroclitus) inhabiting a marine superfund site: in vivo and in vitro studies on the inducibility of xenobiotic metabolizing enzymes. Toxicol Sci 60:77–91

    CAS  PubMed  Google Scholar 

  • Berg MP, Kiers ET, Driessen G, van der Heijden M, Kooi BW, Kuenen F, Liefting M, Verhoef HA, Ellers J (2010) Adapt or disperse: understanding species persistence in a changing world. Glob Change Biol 16:587–598

    Google Scholar 

  • Bernardi G, Fernandez-Delgado C, Gomez-Chiarri M, Powers DA (1995) Origin of a Spanish population of Fundulus heteroclitus inferred by cytochrome b sequence analysis. J Fish Biol 47:737–740

    CAS  Google Scholar 

  • Bickham JW (2011) The four cornerstones of evolutionary toxicology. Ecotoxicology 20:497–502

    CAS  PubMed  Google Scholar 

  • Bickham JW, Sandhu S, Hebert PDN, Chikhi L, Athwal R (2000) Effects of chemical contaminants an genetic diversity in natural populations: implications for biomonitoring and ecotoxicology. Mutat Res 463:33–51

    CAS  PubMed  Google Scholar 

  • Bickham JW, Smolen MJ (1994) Somatic and heritable effects of environmental genotoxins and the emergence of evolutionary toxicology. Environ Health Perspect 102:25–28

    PubMed  PubMed Central  Google Scholar 

  • Billiard SM, Meyer JN, Wassenberg DM, Hodson PV, Di Giulio RT (2008) Nonadditive effects of PAHs on early vertebrate development: mechanisms and implications for risk assessment. Toxicol Sci 105:5–23

    CAS  PubMed  Google Scholar 

  • Billiard SM, Timme-Laragy AR, Wassenberg DM, Cockman C, Di Giulio RT (2006) The role of the aryl hydrocarbon receptor pathway in mediating synergistic developmental toxicity of polycyclic aromatic hydrocarbons to zebrafish. Toxicol Sci 92:526–536

    CAS  PubMed  Google Scholar 

  • Boughman JW (2001) Divergent sexual selection enhances reproductive isolation in sticklebacks. Nature 411:944–948

    CAS  PubMed  Google Scholar 

  • Bozinovic G, Oleksiak MF (2010) Embryonic gene expression among pollutant resistant and sensitive Fundulus heteroclitus populations. Aquat Toxicol 98:221–229

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bozinovic G, Oleksiak MF (2011) Genomic approaches with natural fish populations from polluted environments. Environ Toxicol Chem 30:283–289

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bozinovic G, Sit TL, Di Giulio R, Wills LF, Oleksiak MF (2013) Genomic and physiological responses to strong selective pressure during late organogenesis: few gene expression changes found despite striking morphological differences. BMC Genomics 14:15

    Google Scholar 

  • Burkhart JG, Helgen JC, Fort DJ, Gallagher K, Bowers D, Propst TL, Gernes M, Magner J, Shelby MD, Lucier G (1998) Induction of mortality and malformation in Xenopus laevis embryos by water sources associated with field frog deformities. Environ Health Perspect 106:841–848

    CAS  PubMed  PubMed Central  Google Scholar 

  • Burnett KG, Bain LJ, Baldwin WS, Callard GV, Cohen S, Di Giulio RT, Evans DH, Gomez-Chiarri M, Hahn ME, Hoover CA, Karchner SI, Katoh F, MacLatchy DL, Marshall WS, Meyer JN, Nacci DE, Oleksiak MF, Rees BB, Singer TD, Stegeman JJ, Towle DW, Van Veld PA, Vogelbein WK, Whitehead A, Winn RN, Crawford DL (2007) Fundulus as the premier teleost model in environmental biology: opportunities for new insights using genomics. Comp Biochem Physiol D Genomics Proteomics 2:257–286

    PubMed  Google Scholar 

  • Carney SA, Peterson RE, Heideman W (2004) 2,3,7,8-tetrachlorodibenzo-p-dioxin activation of the aryl hydrocarbon receptor/aryl hydrocarbon receptor nuclear translocator pathway causes developmental toxicity through a CYP1A-independent mechanism in zebrafish. Mol Pharmacol 66:512–521

    CAS  PubMed  Google Scholar 

  • Chan WK, Yao G, Gu YZ, Bradfield CA (1999) Cross-talk between the aryl hydrocarbon receptor and hypoxia inducible factor signaling pathways – demonstration of competition and compensation. J Biol Chem 274:12115–12123

    CAS  PubMed  Google Scholar 

  • Chown SL, Gaston KJ (2008) Macrophysiology for a changing world. Proc R Soc B Biol Sci 275:1469–1478

    Google Scholar 

  • Clark BW, Bone AJ, Di Giulio RT (2013a) Resistance to teratogenesis by F1 and F2 embryos of PAH-adapted Fundulus heteroclitus is strongly inherited despite reduced recalcitrance of the AHR pathway. Environ Sci Pollut Res Int 21(24):13898–13908

    PubMed  PubMed Central  Google Scholar 

  • Clark BW, Cooper EM, Stapleton HM, Di Giulio RT (2013b) Compound- and mixture-specific differences in resistance to polycyclic aromatic hydrocarbons and PCB-126 among Fundulus heteroclitus subpopulations throughout the Elizabeth River Estuary (Virginia, USA). Environ Sci Technol 47:10556–10566

    CAS  PubMed  PubMed Central  Google Scholar 

  • Clark BW, Di Giulio RT (2012) Fundulus heteroclitus adapted to PAHs are cross-resistant to multiple insecticides. Ecotoxicology 21:465–474

    CAS  PubMed  Google Scholar 

  • 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 99:232–240

    CAS  PubMed  PubMed Central  Google Scholar 

  • Coleman ML, Chisholm SW (2010) Ecosystem-specific selection pressures revealed through comparative population genomics. Proc Natl Acad Sci 107:18634–18639

    CAS  PubMed  Google Scholar 

  • Cotter KA, Nacci D, Champlin D, Chuprin J, Callard GV (2015) Cloning of multiple ERalpha mRNA variants in killifish (Fundulus heteroclitus), and differential expression by tissue type, stage of reproduction, and estrogen exposure in fish from polluted and unpolluted environments. Aquat Toxicol 159:184–197

    CAS  PubMed  Google Scholar 

  • Cotter KA, Nacci D, Champlin D, Yeo AT, Gilmore TD, Callard GV (2016) Adaptive significance of ER alpha splice variants in killifish (Fundulus heteroclitus) resident in an estrogenic environment. Endocrinology 157:2294–2308

    CAS  PubMed  Google Scholar 

  • De Coninck DIM, Janssen CR, De Schamphelaere KAC (2014) An approach to assess the regulatory relevance of microevolutionary effects in ecological risk assessment of chemicals: a case study with cadmium. Environ Toxicol Chem 33:453–457

    PubMed  Google Scholar 

  • Di Giulio RT, Clark BW (2015) The Elizabeth River story: a case study in evolutionary toxicology. J Toxicol Env Health B Crit Rev 18:259–298

    Google Scholar 

  • 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 45:99–113

    CAS  Google Scholar 

  • Fleming CR, Matson CW, Hinton DE, Di Giulio RT (2008) Developmental and molecular interactions between hypoxia and aryl hydrocarbon receptor (AHR) pathways in Zebrafish (Danio rerio) and Atlantic killifish (Fundulus heteroclitus). Mar Environ Res 66:72–72

    Google Scholar 

  • Fukunaga BN, Probst MR, Reisz-Porszasz S, Hankinson O (1995) Identification of functional domains of the aryl hydrocarbon receptor. J Biol Chem 270:29270–29278

    CAS  PubMed  Google Scholar 

  • Gilbert SF (2001) Ecological developmental biology: developmental biology meets the real world. Dev Biol 233:1–12

    CAS  PubMed  Google Scholar 

  • Gonzalez I, Levin M, Jermanus S, Watson B, Gilg MR (2009) Genetic assessment of species ranges in Fundulus heteroclitus and F. grandis in northeastern Florida salt marshes. Southeast Nat 8:227–244

    Google Scholar 

  • Grans J, Wassmur B, Fernandez-Santoscoy M, Zanette J, Woodin BR, Karchner SI, Nacci DE, Champlin D, Jayaraman S, Hahn ME, Stegeman JJ, Celander MC (2015) Regulation of pregnane-X-receptor, CYP3A and P-glycoprotein genes in the PCB-resistant killifish (Fundulus heteroclitus) population from New Bedford Harbor. Aquat Toxicol 159:198–207

    PubMed  Google Scholar 

  • Greytak SR, Tarrant AM, Nacci D, Hahn ME, Callard GV (2010) Estrogen responses in killifish (Fundulus heteroclitus) from polluted and unpolluted environments are site- and gene-specific. Aquat Toxicol 99:291–299

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hahn ME (2001) Dioxin toxicology and the aryl hydrocarbon receptor: insights from fish and other non-traditional models. Mar Biotechnol 3:S224–S238

    CAS  PubMed  Google Scholar 

  • Hahn ME (2002) Aryl hydrocarbon receptors: diversity and evolution. Chem Biol Interact 141:131–160

    CAS  PubMed  Google Scholar 

  • Hankinson O (1995) The aryl-hydrocarbon receptor complex. Annu Rev Pharmacol Toxicol 35:307–340

    CAS  PubMed  Google Scholar 

  • Harbeitner RC, Hahn ME, Timme-Laragy AR (2013) Differential sensitivity to pro-oxidant exposure in two populations of killifish (Fundulus heteroclitus). Ecotoxicology 22:387–401

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hawkins RD, Hon GC, Ren B (2010) Next-generation genomics: an integrative approach. Nat Rev Genet 11:476–486

    CAS  PubMed  PubMed Central  Google Scholar 

  • Howell NL, Rifai HS, Koenig L (2011) Comparative distribution, sourcing, and chemical behavior of PCDD/Fs and PCBs in an estuary environment. Chemosphere 83:873–881

    CAS  PubMed  Google Scholar 

  • Howell NL, Suarez MP, Rifai HS, Koenig L (2008) Concentrations of polychlorinated biphenyls (PCBs) in water, sediment, and aquatic biota in the Houston Ship Channel, Texas. Chemosphere 70:593–606

    CAS  PubMed  Google Scholar 

  • Incardona JP, Collier TK, Scholz NL (2004) Defects in cardiac function precede morphological abnormalities in fish embryos exposed to polycyclic aromatic hydrocarbons. Toxicol Appl Pharmacol 196:191–205

    CAS  Google Scholar 

  • Johnson MTJ, Munshi-South J (2017) Evolution of life in urban environments. Science 358(6363):eaam8327

    PubMed  Google Scholar 

  • Jung D, Cho Y, Collins LB, Swenberg JA, Di Giulio RT (2009) Effects of benzo a pyrene on mitochondrial and nuclear DNA damage in Atlantic killifish (Fundulus heteroclitus) from a creosote-contaminated and reference site. Aquat Toxicol 95:44–51

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jung DW, Matson CW, Collins LB, Laban G, Stapleton HM, Bickham JW, Swenberg JA, Di Giulio RT (2011) Genotoxicity in Atlantic killifish (Fundulus heteroclitus) from a PAH-contaminated superfund site on the Elizabeth River, Virginia. Ecotoxicology 20:1890–1899

    CAS  PubMed  PubMed Central  Google Scholar 

  • Karchner SI, Franks DG, Hahn ME (2005) AHR1B, a new functional aryl hydrocarbon receptor in zebrafish: tandem arrangement of ahr1b and ahr2 genes. Biochem J 392:153–161

    CAS  PubMed  PubMed Central  Google Scholar 

  • Karchner SI, Franks DG, Powell WH, Hahn ME (2002) Regulatory interactions among three members of the vertebrate aryl hydrocarbon receptor family: AHR repressor, AHR1, and AHR2. J Biol Chem 277:6949–6959

    CAS  PubMed  Google Scholar 

  • Karchner SI, Powell WH, Hahn ME (1999) Identification and functional characterization of two highly divergent aryl hydrocarbon receptors (AHR1 and AHR2) in the teleost Fundulus heteroclitus – evidence for a novel subfamily of ligand-binding basic helix loop helix-Per-ARNT-Sim (bHLH-PAS) factors. J Biol Chem 274:33814–33824

    CAS  PubMed  Google Scholar 

  • Kawecki TJ, Ebert D (2004) Conceptual issues in local adaptation. Ecol Lett 7:1225–1241

    Google Scholar 

  • Keller R, Davidson LA, Shook DR (2003) How we are shaped: the biomechanics of gastrulation. Differentiation 71:171–205

    PubMed  Google Scholar 

  • Khan AT, Weis JS (1987) Effect of methylmercury on egg and juvenile viability in two populations of killifish Fundulus heteroclitus. Environ Res 44:272–278

    CAS  PubMed  Google Scholar 

  • Kimberly DA, Salice CJ (2015) Evolutionary responses to climate change and contaminants: evidence and experimental approaches. Curr Zool 61:690–701

    Google Scholar 

  • Klerks PL, Xie L, Levinton JS (2011) Quantitative genetics approaches to study evolutionary processes in ecotoxicology; a perspective from research on the evolution of resistance. Ecotoxicology 20:513–523

    CAS  PubMed  Google Scholar 

  • Lakshmanan D, Howell NL, Rifai HS, Koenig L (2010) Spatial and temporal variation of polychlorinated biphenyls in the Houston Ship Channel. Chemosphere 80:100–112

    CAS  PubMed  Google Scholar 

  • Lenormand T (2002) Gene flow and the limits to natural selection. Trends Ecol Evol 17:183–189

    Google Scholar 

  • Lynch M, Conery JS (2003) The origins of genome complexity. Science 302:1401–1404

    CAS  PubMed  Google Scholar 

  • Matson CW, Clark BW, Jenny MJ, Fleming CR, Hahn ME, Di Giulio RT (2008a) Development of the morpholino gene knockdown technique in Fundulus heteroclitus: a tool for studying molecular mechanisms in an established environmental model. Aquat Toxicol 87:289–295

    CAS  PubMed  PubMed Central  Google Scholar 

  • Matson CW, Timme-Laragy AR, Di Giulio RT (2008b) Fluoranthene, but not benzo a pyrene, interacts with hypoxia resulting in pericardial effusion and lordosis in developing zebrafish. Chemosphere 74:149–154

    CAS  PubMed  PubMed Central  Google Scholar 

  • Meaney MJ (2010) Epigenetics and the biological definition of gene x environment interactions. Child Dev 81:41–79

    PubMed  Google Scholar 

  • Meredith WH, Lotrich VA (1979) Production dynamics of a tidal creek population of fundulus-heteroclitus (Linnaeus). Estuar Coast Mar Sci 8:99–118

    Google Scholar 

  • 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 54:621–626

    CAS  PubMed  Google Scholar 

  • Meyer JN, Di Giulio RT (2003) Heritable adaptation and fitness costs in killifish (Fundulus beteroclitus) inhabiting a polluted estuary. Ecol Appl 13:490–503

    Google Scholar 

  • 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 68:69–81

    CAS  PubMed  Google Scholar 

  • Meyer JN, Smith JD, Winston GW, Di Giulio RT (2003a) Antioxidant defenses in killifish (Fundulus heteroclitus) exposed to contaminated sediments and model prooxidants: short-term and heritable responses. Aquat Toxicol 65:377–395

    CAS  PubMed  Google Scholar 

  • Meyer JN, 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

    CAS  PubMed  Google Scholar 

  • Meyer JN, Wassenberg DM, Karchner SI, Hahn ME, Di Giulio RT (2003b) 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

    CAS  PubMed  Google Scholar 

  • 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 134:9–17

    Google Scholar 

  • Nacci DE, Champlin D, Coiro L, McKinney R, Jayaraman S (2002a) Predicting the occurrence of genetic adaptation to dioxinlike compounds in populations of the estuarine fish Fundulus heteroclitus. Environ Toxicol Chem 21:1525–1532

    CAS  PubMed  Google Scholar 

  • Nacci DE, Champlin D, Jayaraman S (2010) Adaptation of the estuarine fish Fundulus heteroclitus (Atlantic killifish) to polychlorinated biphenyls (PCBs). Estuar Coasts 33:853–864

    CAS  Google Scholar 

  • Nacci DE, Kohan M, Pelletier M, George E (2002b) Effects of benzo a pyrene exposure on a fish population resistant to the toxic effects of dioxin-like compounds. Aquat Toxicol 57:203–215

    CAS  PubMed  Google Scholar 

  • Nelson TR, Sutton D, DeVries DR (2014) Summer movements of the Gulf killifish (Fundulus grandis) in a northern Gulf of Mexico salt marsh. Estuar Coasts 37:1295–1300

    Google Scholar 

  • Noury P, Geffard O, Tutundjian R, Garric J (2006) Non destructive in vivo measurement of ethoxyresorufin biotransformation by zebrafish prolarva: development and application. Environ Toxicol 21:324–331

    CAS  PubMed  Google Scholar 

  • Oleksiak MF (2008) Changes in gene expression due to chronic exposure to environmental pollutants. Aquat Toxicol 90:161–171

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 12:263

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Oziolor E, Matson C (2015) Evolutionary toxicology: population adaptation in response to anthropogenic pollution. In: Riesch R, Tobler M, Plath M (eds) Extremophile fishes. Springer, Berlin, pp 247–277

    Google Scholar 

  • Oziolor EM, Bigorgne E, Aguilar L, Usenko S, Matson CW (2014) Evolved resistance to PCB- and PAH-induced cardiac teratogenesis, and reduced CYP1A activity in gulf killifish (Fundulus grandis) populations from the Houston Ship Channel, Texas. Aquat Toxicol 150:210–219

    CAS  PubMed  Google Scholar 

  • Oziolor EM, De Schamphelaere K, Matson CW (2016a) Evolutionary toxicology: meta-analysis of evolutionary events in response to chemical stressors. Ecotoxicology 25:1–9

    Google Scholar 

  • Oziolor EM, Dubansky B, Burggren WW, Matson CW (2016b) Cross-resistance in gulf killifish (Fundulus grandis) populations resistant to dioxin-like compounds. Aquat Toxicol 175:222–231

    CAS  PubMed  Google Scholar 

  • Pal A, He YL, Jekel M, Reinhard M, Gin KYH (2014) Emerging contaminants of public health significance as water quality indicator compounds in the urban water cycle. Environ Int 71:46–62

    CAS  PubMed  Google Scholar 

  • Parmesan C, Yohe G (2003) A globally coherent fingerprint of climate change impacts across natural systems. Nature 421:37–42

    CAS  PubMed  Google Scholar 

  • Poloczanska ES, Brown CJ, Sydeman WJ, Kiessling W, Schoeman DS, Moore PJ, Brander K, Bruno JF, Buckley LB, Burrows MT, Duarte CM, Halpern BS, Holding J, Kappel CV, O'Connor MI, Pandolfi JM, Parmesan C, Schwing F, Thompson SA, Richardson AJ (2013) Global imprint of climate change on marine life. Nat Clim Chang 3:919–925

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Reid NM, Jackson CE, Gilbert D, Minx P, Montague MJ, Hampton TH, Helfrich LW, King BL, Nacci DE, Aluru N, Karchner SI, Colbourne JK, Hahn ME, Shaw JR, Oleksiak MF, Crawford DL, Warren WC, Whitehead A (2017) The landscape of extreme genomic variation in the highly adaptable Atlantic killifish. Genome Biol Evol 9:659–676

    CAS  PubMed Central  Google Scholar 

  • Reid NM, Proestou DA, Clark BW, Warren WC, Colbourne JK, Shaw JR, Karchner SI, Hahn ME, Nacci D, Oleksiak MF, Crawford DL, Whitehead A (2016) The genomic landscape of rapid repeated adaptation to human-altered environments. Science 354:1305–1308

    CAS  PubMed  PubMed Central  Google Scholar 

  • Reitzel AM, Karchner SI, Franks DG, Evans BR, Nacci D, Champlin D, Vieira VM, Hahn ME (2014) Genetic variation at aryl hydrocarbon receptor (AHR) loci in populations of Atlantic killifish (Fundulus heteroclitus) inhabiting polluted and reference habitats. BMC Evol Biol 14:6

    PubMed  PubMed Central  Google Scholar 

  • Rundle HD, Nosil P (2005) Ecological speciation. Ecol Lett 8:336–352

    Google Scholar 

  • Schlezinger JJ, Struntz WDJ, Goldstone JV, Stegeman JJ (2006) Uncoupling of cytochrome P450 1A and stimulation of reactive oxygen species production by co-planar polychlorinated biphenyl congeners. Aquat Toxicol 77:422–432

    CAS  PubMed  Google Scholar 

  • Schmidt JV, Bradfield CA (1996) Ah receptor signaling pathways. Annu Rev Cell Dev Biol 12:55–89

    CAS  PubMed  Google Scholar 

  • Skinner MA, Courtenay SC, Parker WR, Curry RA (2005) Site fidelity of mummichogs (Fundulus heteroclitus) in an Atlantic Canadian estuary. Water Qual Res J Canada 40:288–298

    CAS  Google Scholar 

  • Skinner MA, Courtenay SC, Parker WR, Curry RA (2012) Stable isotopic assessment of site fidelity of mummichogs, Fundulus heteroclitus, exposed to multiple anthropogenic inputs. Environ Biol Fish 94:695–706

    Google Scholar 

  • Smith GM, Weis JS (1997) Predator-prey relationships in mummichogs (Fundulus heteroclitus (L)): effects of living in a polluted environment. J Exp Mar Biol Ecol 209:75–87

    Google Scholar 

  • Stearns S (1993) The evolutionary links between fixed and variable traits. Acta Palaeontol Pol 38:215–232

    Google Scholar 

  • Stegeman JJ (1993) The cytochromes P450 in fish. Elsevier, Amsterdam and New York

    Google Scholar 

  • Stocum DL (2000) Frog limb deformities: an “eco-devo” riddle wrapped in multiple hypotheses surrounded by insufficient data. Teratology 62:147–150

    CAS  PubMed  Google Scholar 

  • Sultan SE (2007) Development in context: the timely emergence of eco-devo. Trends Ecol Evol 22:575–582

    PubMed  Google Scholar 

  • Tang J, Cao Y, Rose RL, Hodgson E (2002) In vitro metabolism of carbaryl by human cytochrome P450 and its inhibition by chlorpyrifos. Chem Biol Interact 141:229–241

    CAS  PubMed  Google Scholar 

  • Theodorakis CW, Shugart LR (1997) Genetic ecotoxicology II: population genetic structure in mosquitofish exposed in situ to radionuclides. Ecotoxicology 6:335–354

    CAS  Google Scholar 

  • Valiela I, Wright JE, Teal JM, Volkmann SB (1977) Growth, production and energy transformations in the salt-marsh killifish Fundulus heteroclitus. Mar Biol 40:135–144

    Google Scholar 

  • Van den Berg M, Birnbaum L, Bosveld ATC, Brunstrom B, Cook P, Feeley M, Giesy JP, Hanberg A, Hasegawa R, Kennedy SW, Kubiak T, Larsen JC, van Leeuwen FXR, Liem AKD, Nolt C, Peterson RE, Poellinger L, Safe S, Schrenk D, Tillitt D, Tysklind M, Younes M, Waern F, Zacharewski T (1998) Toxic equivalency factors (TEFs) for PCBs, PCDDs, PCDFs for humans and wildlife. Environ Health Perspect 106:775–792

    PubMed  PubMed Central  Google Scholar 

  • Van Veld PA, Vogelbein WK, Smolowitz R, Woodin BR, Stegeman JJ (1992) Cytochrome P450IA1 in hepatic lesions of a teleost fish (Fundulus heteroclitus) collected from a polycyclic aromatic hydrocarbon-contaminated site. Carcinogenesis 13:505–507

    PubMed  Google Scholar 

  • Van Veld PA, Westbrook DJ (1995) Evidence for depression of cytochrome P4501A in population of chemically resistant mummichog (Fundulus heteroclitus). Environ Sci 3:221–234

    Google Scholar 

  • Visser ME (2008) Keeping up with a warming world; assessing the rate of adaptation to climate change. Proc R Soc B Biol Sci 275:649–659

    Google Scholar 

  • Vogelbein WK, Fournie JW, Van Veld PA, Huggett RJ (1990) Hepatic neoplasms in the mummichog Fundulus heteroclitus from a creosote-contaminated site. Cancer Res 50:5978–5986

    CAS  PubMed  Google Scholar 

  • Wang GL, Jiang B-H, Rue EA, Semenza GL (1995) Hypoxia-inducible factor 1 is a basic-helix-loop-helix-PAS heterodimer regulated by cellular O-2 tension. Proc Natl Acad Sci U S A 92:5510–5514

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wassenberg DM, Di Giulio RT (2004a) Synergistic embryotoxicity of polycyclic aromatic hydrocarbon aryl hydrocarbon receptor agonists with cytochrome P4501A inhibitors in Fundulus heteroclitus. Environ Health Perspect 112:1658–1664

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wassenberg DM, Di Giulio RT (2004b) Teratogenesis in Fundulus heteroclitus embryos exposed to a creosote-contaminated sediment extract and CYP1A inhibitors. Mar Environ Res 58:163–168

    CAS  PubMed  Google Scholar 

  • Wassenberg DM, Nerlinger AL, Battle LP, Di Giulio RT (2005) Effects of the polycyclic aromatic hydrocarbon heterocycles, carbazole and dibenzothiophene, on in vivo and in vitro CYP1A activity and polycyclic aromatic hydrocarbon-derived embryonic deformities. Environ Toxicol Chem 24:2526–2532

    CAS  PubMed  Google Scholar 

  • Wassenberg DM, Swails EE, Di Giulio RT (2002) Effects of single and combined exposures to benzo(a)pyrene and 3,3′ 4,4′ 5-pentachlorobiphenyl on EROD activity and development in Fundulus heteroclitus. Mar Environ Res 54:279–283

    CAS  PubMed  Google Scholar 

  • Weis JS, Khan AA (1990) Effects of mercury on feeding behavior of the mummichog, Fundulus heteroclitus from a polluted habitat. Mar Environ Res 30:243–249

    CAS  Google Scholar 

  • Weis JS, Weis P (1995) Swimming performance and predator avoidance by mummichog (Fundulus heteroclitus) larvae after embryonic or larval exposure to methylmercury. Can J Fish Aquat Sci 52:2168–2173

    CAS  Google Scholar 

  • Weis JS, Weis P, Heber M, Vaidya S (1981a) Methylmercury tolerance of killifish (Fundulus heteroclitus) embryos from a polluted vs non-polluted environment. Mar Biol 65:283–287

    CAS  Google Scholar 

  • Weis P (1984) Metallothionein and mercury tolerance in the killifish, fundulus-heteroclitus. Mar Environ Res 14:153–166

    CAS  Google Scholar 

  • Weis P, Weis JS (1977) Methylmercury teratogenesis in the killifish, Fundulus heteroclitus. Teratology 16:317–325

    CAS  PubMed  Google Scholar 

  • Weis P, Weis JS, Heber MA (1981b) Variation in teratogenic response to methylmercury by killifish (Fundulus heteroclitus) embryos – differences within and between populations. Anat Rec 199:A270–A271

    Google Scholar 

  • Whitehead A (2010) The evolutionary radiation of diverse osmotolerant physiologies in killifish (Fundulus sp.) Evolution 64:2070–2085

    PubMed  Google Scholar 

  • Whitehead A, Pilcher W, Champlin D, Nacci D (2012) Common mechanism underlies repeated evolution of extreme pollution tolerance. Proc R Soc B Biol Sci 279:427–433

    Google Scholar 

  • Williams LM, Oleksiak MF (2008) Signatures of selection in natural populations adapted to chronic pollution. BMC Evol Biol 8:282

    PubMed  PubMed Central  Google Scholar 

  • Williams LM, Oleksiak MF (2011a) Ecologically and evolutionarily important SNPs identified in natural populations. Mol Biol Evol 28:1817–1826

    CAS  PubMed  PubMed Central  Google Scholar 

  • Williams LM, Oleksiak MF (2011b) Evolutionary and functional analyses of cytochrome P4501A promoter polymorphisms in natural populations. Mol Ecol 20:5236–5247

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wills LP, Jung D, Koehrn K, Zhu SQ, Willett KL, Hinton DE, Di Giulio RT (2010a) Comparative chronic liver toxicity of Benzo a pyrene in two populations of the Atlantic killifish (Fundulus heteroclitus) with different exposure histories. Environ Health Perspect 118:1376–1381

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wills LP, Matson CW, Landon CD, Di Giulio RT (2010b) Characterization of the recalcitrant CYP1 phenotype found in Atlantic killifish (Fundulus heteroclitus) inhabiting a superfund site on the Elizabeth River, VA. Aquat Toxicol 99:33–41

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wills LP, Zhu SQ, Willett KL, Di Giulio RT (2009) Effect of CYP1A inhibition on the biotransformation of benzo[a]pyrene in two populations of Fundulus heteroclitus with different exposure histories. Aquat Toxicol 92:195–201

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 331:1322–1325

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wirgin I, Waldman JR (2004) Resistance to contaminants in North American fish populations. Mutat Res 552:73–100

    CAS  PubMed  Google Scholar 

  • Yuan ZP, Courtenay S, Chambers RC, Wirgin I (2006) Evidence of spatially extensive resistance to PCBs in an anadromous fish of the Hudson River. Environ Health Perspect 114:77–84

    CAS  PubMed  Google Scholar 

  • Zhou T, Scali R, Weis P, Weis JS (1996) Behavioral effects in mummichog larvae (Fundulus heteroclitus) following embryonic exposure to methylmercury. Mar Environ Res 42:45–49

    CAS  Google Scholar 

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Authors and Affiliations

  1. Department of Environmental Science, Center for Reservoir and Aquatic Systems Research (CRASR), Institute for Biomedical Studies, Baylor University, Waco, TX, USA

    Elias M. Oziolor & Cole W. Matson

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  1. Elias M. Oziolor
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  2. Cole W. Matson
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Correspondence to Cole W. Matson .

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  1. University of North Texas, Department of Biological Sciences, Denton, TX, USA

    Warren Burggren

  2. University of North Texas, Department of Biological Sciences, Denton, TX, USA

    Benjamin Dubansky

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Oziolor, E.M., Matson, C.W. (2018). Adaptation in Polluted Waters: Lessons from Killifish. In: Burggren, W., Dubansky, B. (eds) Development and Environment. Springer, Cham. https://doi.org/10.1007/978-3-319-75935-7_14

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