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Adaptation of the Estuarine Fish Fundulus heteroclitus (Atlantic Killifish) to Polychlorinated Biphenyls (PCBs)

Abstract

In this study, we describe remarkable intraspecific variation in sensitivity to the broadly distributed pollutants, polychlorinated biphenyls (PCBs), among wild populations of the nonmigratory estuarine Atlantic killifish (Fundulus heteroclitus). Variation among killifish populations was characterized in 28-day laboratory challenges using embryonic and larval life stages and the highly toxic, dioxin-like PCB congener, 3,3′4,4′,5-hexachlorobiphenyl (PCB126). In summarizing results for 24 populations, we show that killifish populations vary over four orders of magnitude in their sensitivity to PCB126 and that this variation is adaptive to the magnitude of contamination at their residence site. The four least-sensitive killifish populations reside in US Atlantic coast urban harbors >100 km apart from one another: New Bedford, MA, Bridgeport, CT, Newark, NJ, and Norfolk, VA, USA. Prior studies examining all but the CT population have shown that these killifish are relatively insensitive to local contaminants, with mixed evidence concerning the heritability of this trait. We show here that tolerance to PCB126 is extreme, with some mechanistic similarities among these four killifish populations. However, these populations do not respond identically to each other, and in at least one population, tolerance appears to degrade over the F1 and F2 generations tested. Complementary ongoing studies using molecular approaches provide opportunity to identify unique and shared mechanisms of tolerance in these independently evolving populations and explore the adaptive benefits and costs of contemporary evolutionary responses in the wild.

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References

  • Adams, S.M., J.B. Lindmeier, and D.D. Duvernell. 2006. Microsatellite analysis of the phylogeography, Pleistocene history and secondary contract hypotheses for the killifish, Fundulus heteroclitus. Molecular Ecology 15(4): 1109–1123.

    Article  CAS  Google Scholar 

  • Andreason, E.A., J.M. Spitsbergen, R.L. Tanguay, J.J. Stegeman, W. Heideman, and R.E. Peterson. 2002. Tissue-specific expression of AHR2, ARNT2, and CYP1A in zebrafish embryos and larvae: Effects of developmental stage and 2, 3, 7, 8-tetrachlorodibenzo-p-dioxin exposure. Toxicological Sciences 68: 403–419.

    Article  Google Scholar 

  • Bello, S.M., D.G. Franks, J.J. Stegeman, and M.E. Hahn. 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. Toxicological Sciences 60: 77–91.

    Article  CAS  Google Scholar 

  • Bieri, R.H., C. Hein, R.J. Huggett, P. Shou, H. Slone, C. Smith, and C.-W. Su. 1986. Polycyclic aromatic hydrocarbons in surface sediments from the Elizabeth River subestuary. International Journal of Environmental Analytical Chemistry 26: 97–113.

    Article  CAS  Google Scholar 

  • Billiard, S.M., A.R. Timme-Laragy, D.M. Wassenberg, C. Cockman, and R.T. Di Giulio. 2006. The role of the aryl hydrocarbon receptor pathway in mediating synergistic developmental toxicity of polycyclic aromatic hydrocarbons to zebrafish. Toxicological Sciences 92(2): 526–536.

    Article  CAS  Google Scholar 

  • Bruce, R.D., and D.J. Versteeg. 1992. A statistical procedure for modeling continuous toxicity data. Environmental Toxicology and Chemistry 11: 1485–1494.

    Article  CAS  Google Scholar 

  • Bunger, M.K., E. Glover, S.M. Moran, J.A. Walisser, G.P. Lahvis, E.L. Hsu, and C.A. Bradfield. 2008. Abnormal liver development and resistance to 2, 3, 7, 8-tetrachloro-p-dioxin toxicity in mice carrying a mutation in the DNA-binding domain of the aryl hydrocarbon receptor. Toxicological Sciences 106(1): 83–92.

    Article  CAS  Google Scholar 

  • Burnett, K.G., L.J. Bain, W.S. Baldwin, G.V. Callard, S. Cohen, D. Giulio, D.H. Evans, M. Gomez-Chiarri, M.E. Hahn, C.A. Hoover, S.I. Karchner, F. Katoh, D.L. MacLatchy, W.S. Marshall, J.N. Meyer, D.E. Nacci, M.F. Oleksiak, B.B. Rees, T.P. Singer, J.J. Stegeman, D.W. Towle, P.A. Van Veld, W.K. Vogelbein, A. Whitehead, R. Winn, and D.L. Crawford. 2007. Fundulus as the premier teleost model in environmental biology: Opportunities for new insights using genomics. Comparative Biochemistry and Physiology, Part D 2: 257–286.

    Google Scholar 

  • Cantrell, S.M., L.H. Lutz, D.E. Tillitt, and M. Hannink. 1996. Embryotoxicity of 2, 3, 7, 8 tetrachlorodibenzo-p-dioxin (TCDD): The embryonic vasculature is a physiological target for TCDD-induced DNA damage and apoptotic cell death in medaka (Oryzias latipes). Toxicology and Applied Pharmacology 141: 23–34.

    CAS  Google Scholar 

  • Carney, S.A., R.E. Peterson, and W. Heideman. 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. Molecular Pharmacology 66: 512–521.

    CAS  Google Scholar 

  • Cohen, C.S., J. Tirindelli, M. Gomez-Chiarri, and D. Nacci. 2006. Functional implications of major histocompatibility variation using estuarine fish populations. Integrative & Comparative Biology 46(6): 1016–1029.

    Article  CAS  Google Scholar 

  • Crawford, D.W., N.L. Bonnevie, and R.J. Wenning. 1995. Sources of pollution and sediment contamination in Newark Bay, New Jersey. Ecotoxicology and Environmental Safety 30(1): 85–100.

    Article  CAS  Google Scholar 

  • Duvernell, D.D., J.B. Lindmeier, K.E. Faust, and A. Whitehead. 2008. Relative influences of historical and contemporary forces shaping the distribution of genetic variation in the Atlantic killifish, Fundulus heteroclitus. Molecular Ecology 17: 1344–1360.

    Article  Google Scholar 

  • Ellegren, H., and B.C. Sheldon. 2008. Genetic basis of fitness differences in natural populations. Nature 452: 169–175.

    Article  CAS  Google Scholar 

  • Elskus, A.A., E. Monosson, A.E. McElroy, J.J. Stegeman, and D.S. Woltering. 1999. Altered CYP1A expression in Fundulus heteroclitus adults and larvae: A sign of pollution resistance? Aquatic Toxicology 45: 99–113.

    Article  CAS  Google Scholar 

  • Fisher, M.A., and M.F. Oleksiak. 2007. Convergence and divergence in gene expression among natural populations exposed to pollution. BMC Genomics 8: 108–118.

    Article  Google Scholar 

  • Frederick, L.A., P.A. Van Veld, and C.D. Rice. 2007. Bioindicators of immune function in creosote-adapted estuarine killifish, Fundulus heteroclitus. Journal of Toxicology and Environmental Health Part A 70(17): 1433–1442.

    Article  CAS  Google Scholar 

  • Hahn, M.E. 2002. Biomarkers and bioassays for detecting dioxin-like compounds in the marine environment. Science of the Total Environment 289: 49–69.

    Article  CAS  Google Scholar 

  • Hahn, M.E., S.I. Karchner, D.G. Franks, and R.R. Merson. 2004. Aryl hydrocarbon receptor polymorphisms and dioxin resistance in Atlantic killifish. Pharmacogenetics 14: 131–143.

    Article  CAS  Google Scholar 

  • Hahn, M.E., S.I. Karchner, B.R. Evans, D.G. Franks, R.R. Merson, and J.M. Lapseritis. 2006. Unexpected diversity of aryl hydrocarbon receptors in non-mammalian vertebrates. Journal of Experimental Zoology Part A Comparative and Experimental Biology 305: 693–706.

    Article  Google Scholar 

  • Head, J.A., M.E. Hahn, and S.W. Kennedy. 2008. Key amino acids in the aryl hydrocarbon receptor predict dioxin sensitivity in avian species. Environmental Science and Technology 42: 7535–7541.

    Article  CAS  Google Scholar 

  • Institute S.A.S. 2001. SAS/STAT users guide, version 8. Cary: SAS.

    Google Scholar 

  • Jayaraman, S., D.E. Nacci, D.M. Champlin, R.J. Pruell, K.J. Rocha, C.M. Custer, T.W. Custer, and M. Cantwell. 2009. PCBs and DDE in tree swallow (Tachycineta bicolor) eggs and nestlings from an estuarine PCB Superfund site, New Bedford Harbor, MA, USA. Environmental Science and Technology 43: 8387–8392.

    Article  CAS  Google Scholar 

  • Karchner, S.I., W.H. Powell, and M.E. Hahn. 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. Journal of Biological Chemistry 274: 33814–33824.

    Article  CAS  Google Scholar 

  • Lauenstein, G. G., and A. Y. Cantillo. 1993. Sampling and analytical methods of the National Status and trends Program National Benthic Surveillance and Mussel Watch Projects. Volume I: Overview and Summary of Methods. NOAA Technical Memorandum NOS ORCA 71.

  • Lauenstein, G.G., and K.L. Kimbrough. 2007. Chemical contamination of the Hudson–Raritan Estuary as a result of the attack on the World Trade Center: Analysis of polychlorinated aromatic hydrocarbons and polychlorinated biphenyls in mussels and sediment. Marine Pollution Bulletin 54: 284–294.

    Article  CAS  Google Scholar 

  • Long, E.R., D.D. McDonald, S.L. Smith, and F.D. Calder. 1995. Incidence of adverse biological effects within ranges of chemical concentrations in marine and estuarine sediments. Environmental Management 19: 81–97.

    Article  Google Scholar 

  • Matson, C.W., B.W. Clark, M.J. Jenny, C.R. Fleming, M.E. Hahn, and R.T. Di Giulio. 2008. Development of the morpholino gene knockdown technique in Fundulus heteroclitus: A tool for studying molecular mechanisms in an established environmental model. Aquatic Toxicology 87: 289–295.

    Article  CAS  Google Scholar 

  • McMillan, A.M., M.J. Bagley, S.A. Jackson, and D.E. Nacci. 2006. Genetic diversity and structure of an estuarine fish (Fundulus heteroclitus) indigenous to sites associated with a highly contaminated urban harbor. Ecotoxicology 15: 539–548.

    Article  CAS  Google Scholar 

  • Meyer, J.N., and R.T. Di Giulio. 2003. Heritable adaptation and fitness costs in killifish (Fundulus heteroclitus) inhabiting a polluted estuary. Ecological Applications 13(2): 490–503.

    Article  Google Scholar 

  • Meyer, J.N., D.E. Nacci, and R.T. Di Giulio. 2002. Cytochrome P450A(CYP1A) in killifish (Fundulus heteroclitus): Heritability of altered expression and relationship to survival in contaminated sediments. Toxicological Sciences 68: 69–81.

    Article  CAS  Google Scholar 

  • Meyer, J.N., D.M. Wassenberg, S.I. Karchner, M.E. Hahn, and R.T. Di Giulio. 2003. Expression and inducibility of aryl hydrocarbon receptor pathway genes in wild-caught killifish (Fundulus heteroclitus) with contaminant-exposure histories. Environmental Toxicology and Chemistry 22(10): 2337–2343.

    Article  CAS  Google Scholar 

  • Miller, M.R., J.P. Dunham, W.A. Amores, W.A. Cresko, and E.A. Johnson. 2007. Rapid and cost-effective polymorphism identification and genotyping using restriction site associated DNA (RAD) markers. Genome Research 17: 240–248.

    Article  CAS  Google Scholar 

  • Mitton, J.B. 1994. Selection in natural populations. New York: Oxford University Press.

    Google Scholar 

  • Mulvey, M., M.C. Newman, W. Vogelbein, M.A. Unger, and D.R. Ownby. 2003. Genetic structure and mtDNA diversity of Fundulus heteroclitus populations from polycyclic aromatic hydrocarbon-contaminated sites. Environmental Toxicology and Chemistry 22: 671–677.

    CAS  Google Scholar 

  • Nacci, D., L. Coiro, D. Champlin, S. Jayaraman, R. McKinney, T. Gleason, W.R. Munns Jr., J. Specker, and K. Cooper. 1999. Adaptation of wild fish populations to dioxin-like environmental contamination. Marine Biology 134: 9–17.

    Article  Google Scholar 

  • Nacci, D., L. Coiro, D. Champlin, S. Jayaraman, and R. McKinney. 2002a. Predicting the occurrence of genetic adaptation to dioxin-like compounds in populations of the estuarine fish Fundulus heteroclitus. Environmental Toxicology and Chemistry 21(7): 1525–1532.

    CAS  Google Scholar 

  • Nacci, D., T. Gleason, R. Gutjahr-Gobell, M. Huber, and W.R. Munns Jr. 2002b. Effects of environmental stressors on wildlife populations. In Coastal and estuarine risk assessment: risk on the edge, ed. M.C. Newman. Washington, DC: CRC/Lewis.

    Google Scholar 

  • Nacci, D., L. Coiro, D. Wasserman, and R. Di Giuilio. 2005. A non-destructive technique to measure cytochrome P4501A enzyme activity in living embryos of the estuarine fish Fundulus heteroclitus. In Techniques in aquatic toxicology, vol. 2, ed. G.K. Ostrander, 209–225. Boca Raton: Taylor and Francis.

    Google Scholar 

  • Nacci, D., M. Huber, D. Champlin, S. Jayaraman, S. Cohen, E. Gauger, A. Fong, and M. Gomez-Chiarri. 2009. Evolution of tolerance to PCBs and susceptibility to a bacterial pathogen (Vibrio harveyi) in Atlantic killifish (Fundulus heteroclitus) from New Bedford (MA, USA) harbor. Environmental Pollution 157: 857–864.

    Article  CAS  Google Scholar 

  • Nelson, W. G., B. J. Bergen, S. J. Benyi, G. Morrison, R. A. Voyer, C. J. Strobel, S. Rego, G. Thursby, and C. E. Pesch. 1996. New Bedford harbor long-term monitoring assessment report: Baseline sampling. US Environmental Protection Agency, National Health and Environmental Effects Research Laboratory, Atlantic Ecology Division, Narragansett, RI. EPA/600/R-96/097.

  • Okey, A.B., M.A. Franc, I.D. Moffat, N. Tijet, P.C. Boutros, M. Korkaainen, J. Tuomisto, and R. Pohjanvirta. 2005. Toxicological implications of polymorphisms in receptors for xenobiotic chemicals: The case of the aryl hydrocarbon receptor. Toxicology and Applied Pharmacology 207: 43–51.

    Article  Google Scholar 

  • Oleksiak, M.F. 2008. Changes in gene expression due to chronic exposure to environmental pollutants. Aquatic Toxicology 90: 161–171.

    Article  CAS  Google Scholar 

  • Ownby, D.R., M.C. Newman, M. Mulvey, W.K. Vogelbein, M.A. Unger, and L.F. Arzayus. 2002. Fish (Fundulus heteroclitus) populations with different exposure histories differ in tolerance of creosote-contaminated sediments. Environmental Toxicology and Chemistry 21(9): 1987–1902.

    Google Scholar 

  • Payne, J.F., A. Mathieu, and T.K. Collier. 2003. Ecotoxicological studies focusing on marine and freshwater fish. In PAHs: An ecotoxicological perspective, ed. P.E.T. Douben, 191–224. Hoboken: Wiley.

    Chapter  Google Scholar 

  • Powell, W.H., R. Bright, S.M. Bello, and M.E. Hahn. 2000. Developmental and tissue-specific expression of AHR1, AHR2, and ARNT2 in dioxin-sensitive and -resistant populations of the marine fish, Fundulus heteroclitus. Toxicological Sciences 57: 229–239.

    Article  CAS  Google Scholar 

  • Prince, R., and K.R. Cooper. 1995. Comparisons of the effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin on chemically-impacted and non-impacted subpopulations of Fundulus heteroclitus: I. TCDD toxicity. Environmental Toxicology and Chemistry 14: 579–588.

    CAS  Google Scholar 

  • Roark, S.A., D. Nacci, L. Coiro, D. Champlin, and S.I. Guttman. 2005. Population genetic structure of a non-migratory marine fish Fundulus heteroclitus across a strong gradient of PCB contamination. Environmental Toxicology and Chemistry 24(3): 717–725.

    Article  CAS  Google Scholar 

  • Rogerson, P.F., S.C. Schimmel, and G. Hoffman. 1985. Chemical and biological characterization of black rock harbor dredged material. D-85-9. Technical Report. Vicksburg: U.S. Army Corps of Engineers.

    Google Scholar 

  • Safe, S. 1990. Polychlorinated biphenyls (PCBs), dibenzo-p-dioxins (PCDDs), dibenzofurans (PCDFs), and related compounds: environmental and mechanistic considerations which support the development of toxic equivalency factors (TEFs). CRC Critical Reviews in Toxicology 21: 51–88.

    Article  CAS  Google Scholar 

  • Teo, S.L.H., and K.W. Able. 2003. Habitat use and movement of the mummichog (Fundulus heteroclitus) in a restored marsh. Estuaries 26: 720–730.

    Article  Google Scholar 

  • Tillitt, D.E., P.M. Cook, J.P. Giesy, W. Heideman, and R.E. Peterson. 2008. Reproductive impairment of Great Lakes lake trout by dioxin-like chemicals. In The toxicology of fishes, ed. R.T. Di Giulio and D.E. Hinton, 819–876. Washington, DC: Taylor and Francis.

    Google Scholar 

  • Tirindelli, J. 2007. A comparison of immunogenetic profiles between PCB contaminated and reference killifish populations. Master of Science. San Francisco State University, San Francisco, CA

  • Van den Berg, M., L. Birnbaum, A.T.C. Bosveld, B. Brunstrom, P. Cook, M. Feely, J.P. Giesy, A. Hanberg, R. Hasegawa, S.W. Kennedy, T. Kubiak, J.C. Larsen, F.X.R. van Leeuwen, A.K. Djien Liem, C. Nolt, R.E. Peterson, L. Poellinger, S. Stephen, D. Schrenk, D. Tillitt, M. Tysklind, M. Younes, F. Wærn, and T. Zacharewsk. 1998. Toxic equivalency factors (TEFs) for PCBs, PCDDs, PCDFs for humans and wildlife. Environmental Health Perspectives 106: 775–792.

    Article  Google Scholar 

  • Van Veld, P.A., and D. Nacci. 2008. Chemical tolerance: Acclimation and adaptations to chemical stress. In The toxicology of fishes, ed. R.T. Di Giulio and D.E. Hinton. Washington, DC: Taylor and Francis.

    Google Scholar 

  • Walker, S.E., R.M. Dickhut, and C. Chisholm-Brause. 2004. Polycyclic aromatic hydrocarbons in a highly industrialized urban estuary: Inventories and trends. Environmental Toxicology and Chemistry 23(11): 2655–2664.

    Article  CAS  Google Scholar 

  • Weis, J.S. 2002. Tolerance to environmental contaminants in the killifish, Fundulus heteroclitus. Human and Ecological Risk Assessment 8(5): 933–953.

    Article  Google Scholar 

  • Whyte, J.J., R.E. Jung, C.J. Scmitt, and D.E. Tillitt. 2000. Ethoxyresorufin-o-deethylase (EROD) activity in fish as a biomarker of chemical exposure. Critical Reviews in Toxicology 30(4): 347–569.

    Article  CAS  Google Scholar 

  • Williams, L.M., and M.F. Oleksiak. 2008. Signatures of selection in natural populations adapted to chronic pollution. BMC Evolutionary Biology 8: 282–294.

    Article  Google Scholar 

  • Wirgin, I., and J.R. Waldman. 2004. Resistance to contaminants in North American fish populations. Mutation Research 55(1–2): 1897–1902.

    Google Scholar 

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Acknowledgements

We appreciate the assistance and encouragement of the staff at Bloodroot Restaurant (Bridgeport, CT), Peter Van Veld (Virginia Institute of Marine Sciences, VA), the technical support of Jane Copeland and James Heltshe, CSC Corporation, as well as helpful advice from reviewers of early drafts, Ruth Gutjahr-Gobell, Marguerite Pelletier, and Eric Waits, US Environmental Protection Agency. We also acknowledge the assistance of anonymous reviewers contributing to the final version of this manuscript. This is contribution number AED-09-014 of the US Environmental Protection Agency, Office of Research and Development, National Health and Environmental Effects Research Laboratory, Atlantic Ecology Division. This manuscript has been reviewed and approved for publication by the US EPA. Approval does not signify that the contents necessarily reflect the views and policies of the US EPA. Mention of trade names, products, or services does not convey and should not be interpreted as conveying official US EPA approval, endorsement, or recommendation.

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Correspondence to Diane E. Nacci.

Appendix

Appendix

Table 3 Characteristics of previously unpublished early life stage exposure-lethality models that describe tolerance to 3,3′4,4′,5-pentachloro biphenyl (PCB126) for progeny of F. heteroclitus from those sites described in Table 1

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Nacci, D.E., Champlin, D. & Jayaraman, S. Adaptation of the Estuarine Fish Fundulus heteroclitus (Atlantic Killifish) to Polychlorinated Biphenyls (PCBs). Estuaries and Coasts 33, 853–864 (2010). https://doi.org/10.1007/s12237-009-9257-6

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Keywords

  • Adaptation
  • Evolution
  • Killifish
  • Polychlorinated biphenyls
  • Dioxin
  • Tolerance
  • Fundulus heteroclitus