Skip to main content
SpringerLink
Log in

Genetic diversity and structure of an estuarine fish (Fundulus heteroclitus) indigenous to sites associated with a highly contaminated urban harbor

  • Published:
Ecotoxicology Aims and scope Submit manuscript

Abstract

Intense selection on isolated populations can cause loss of genetic diversity, which if persistent, reduces adaptive potential and increases extinction probability. Phenotypic evidence of inherited tolerance suggests that polychlorinated biphenyls (PCBs), have acted as strong selective agents on populations of a non-migratory fish, Fundulus heteroclitus, indigenous to heavily contaminated sites. To evaluate population genetic structure and test for effects of intense, multi-generational PCB contamination on genetic diversity, we used AFLP analysis on fish collected from six sites along the east coast of North America that varied widely in PCB contamination. The sites included a heavily contaminated urban harbor (New Bedford, MA), an adjacent moderately contaminated sub-estuary (Buzzards Bay, MA), and an uncontaminated estuary 60 km away (Narragansett, RI). AFLP markers distinguished populations at moderate and small scales, suggesting genetic differentiation at distances of 2 km or less. Genetic diversity did not differ across the study sites. Genome-wide diversity may have been preserved because of large effective population sizes and/or because the mechanism for genetic adaptation to these contaminants affected only a small number of loci. Alternatively, loss in diversity may have been restored with moderate levels of migration and relatively short generation time for this species.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Antonovics J, Bradshaw AD, Turner RG (1971) Heavy metal tolerance in plants. In: Cragg JB (ed) Advances in ecological research, vol 7. Academic Press, London, pp 1–85

    Google Scholar 

  • Bagley MJ, Anderson SL, May B (2001) Choice of methodology for assessing genetic impacts of environmental stressors: polymorphism and reproducibility of RAPD and AFLP fingerprints. Ecotoxicology 10:239–244

    Article  CAS  Google Scholar 

  • Baker R, Lavie B, Nevo E (1985) Natural selection for resistance to mercury pollution. Experientia 41:697–699

    Article  CAS  Google Scholar 

  • Baquero F, Blazquez J (1997) Evolution of antibiotic resistance. Trends Ecol Evol 12:482–487

    Article  Google Scholar 

  • Benton MJ, Diamond SA, Guttman SI (1994) A genetic and morphometric comparison of Helisoma trivolvis and Gambusia holbrooki from clean and contaminated habitats. Ecotoxicol Environ Safe 2:20–37

    Article  Google Scholar 

  • Black DE, Gutjahr-Gobell R, Pruell RJ, Bergen B, Mills L, McElroy AE (1998a) Reproduction and polychlorinated biphenyls in Fundulus heteroclitus (Linnaeus) from New Bedford Harbor, Massachusetts, USA. Environ Toxicol Chem 17:1405–1414

    Article  CAS  Google Scholar 

  • Black DE, Gutjahr-Gobell R, Pruell RJ, Bergen B (1998b) Effects of a mixture of non-ortho and mono-ortho-polychlorinated biphenyls on reproduction in Fundulus heteroclitus (Linnaeus). Environ Toxicol Chem 7:1396–1404

    Article  Google Scholar 

  • Brown BL, Chapman RW (1991) Gene flow and mitochondrial DNA variation in the killifish, Fundulus heteroclitus. Evolution 45:1147–1161

    Article  Google Scholar 

  • Buntjer JB, Otsen M (1999) Cross checker provides computer-assisted marker interpretation. J Agric Genom, http://www.cabi-publishing.org/jag/papers99/paper599/indexp599.html

  • Butner A, Brattsrom BH (1960) Local movement in Menidia and Fundulus. Copeia 2:139–141

    Article  Google Scholar 

  • Coustau C, Chevillon C, French-Constant R (2000) Resistance to xenobiotics and parasites: can we count the costs? Trends Ecol Evol 15:378–383

    Article  Google Scholar 

  • Crow JF (1957) Genetics of insect resistance to chemicals. Annu Rev Entomol 2:227–246

    Article  CAS  Google Scholar 

  • Fisher RA (1930) The genetical theory of natural selection, 1st edn. Clarendon, Oxford

    Google Scholar 

  • Foré SA, Guttman SI, Bailer AJ, Altfater DJ, Counts BV (1995) Exploratory analysis of population genetic assessment as a water quality indicator. I. Pimephales notatus. Ecotoxicol Environ Safe 30:24–35

    Article  Google Scholar 

  • Frankham R (1995) Effective population size/adult population size ratio in wildlife: a review. Genet Res 66:95–107

    Article  Google Scholar 

  • Gillespie RB, Guttman SI (1999) Chemical-induced changes in the genetic structure of populations: effects on allozymes. In: Forbes VE (ed) Genetics and ecotoxicology. Taylor and Francis Inc., Philadelphia, pp 55–77

    Google Scholar 

  • Hahn ME (1998) The aryl hydrocarbon receptor: a comparative perspective. Comp Biochem Physiol Part C 121:23–53

    CAS  Google Scholar 

  • Hedgecock D (1994) Does variance in reproductive success limit effective population sizes of marine organisms? In: Beaumont AR (ed) Genetics and evolution of aquatic organisms. Chapman & Hall, London, pp. 122–134

    Google Scholar 

  • Hedrick PW (1999) Highly variable loci and their interpretation in evolution and conservation. Evolution 53:313–318

    Article  Google Scholar 

  • Heithaus MR, Laushman RH (1997) Genetic variation and conservation of stream fishes: influence of ecology, life history, and water quality. Can J Fish Aquat Sci 54:1822–1836

    Article  Google Scholar 

  • Keklak MM, Newman MC, Mulvey M (1994) Enhanced uranium tolerance of an exposed population of eastern mosquitofish (Gambusia holbrooki Girard 1859). Arch Environ Contam Toxicol 27:20–24

    Article  CAS  Google Scholar 

  • Klerks PL, Levinton JS (1989) Rapid evolution of metal resistance in a benthic oligochaete inhabiting a metal-polluted site. Biol Bull 176:135–141

    Article  CAS  Google Scholar 

  • Kneib RT (1986) The role of Fundulus heteroclitus in salt marsh trophic dynamics. Am Zool 26:259–269

    Google Scholar 

  • Kopp RL, Guttman SI, Wissing TE (1992) Genetic indicators of environmental stress in central mudminnow (Umbra limi) populations exposed to acid deposition in the Adirondack Mountains. Environ Toxicol Chem 11:665–676

    Article  CAS  Google Scholar 

  • Lande R, Shannon S (1996) The role of genetic variation in adaptation and population persistence in a changing environment. Evolution 50:434–437

    Article  Google Scholar 

  • Lavie B, Nevo E (1986) Genetic selection of homozygote allozyme genotypes in marine gastropods exposed to cadmium pollution. Sci Total Environ 57:91–98

    Article  CAS  Google Scholar 

  • Leamon JH (1999) Gene flow and migration in populations of Fundulus heteroclitus macrolepidotus located in southeastern Connecticut. Masters thesis, University of Connecticut, Storrs, CT, USA

  • Leonard AC, Franson SE, Hertzberg VS, Smith MK, Toth GP (1999) Hypothesis testing with the similarity index. Mol Ecol 8:2105–2114

    Article  CAS  Google Scholar 

  • Long ER, MacDonald DD, Smith SL, Calder FD (1995) Incidence of adverse biological effects within ranges of chemical concentrations in marine and estuarine sediments. Environ Manage 19:81–97

    Article  Google Scholar 

  • Lotrich VA (1975) Summer home range and movements of Fundulus heteroclitus (Pisces: Cyprinodontidae) in a tidal creek. Ecology 56:191–198

    Article  Google Scholar 

  • Lynch M (1990) The similarity index and DNA fingerprinting. Mol Biol Evol 7:478–484

    CAS  Google Scholar 

  • Lynch M (1991) Analysis of population genetic structure by DNA fingerprinting. In: Burke T, Dolf G, Jeffreys AJ, Wolff R (eds) DNA fingerprinting: approaches and applications. Birkhauser-Verlag, Basel, Switzerland, pp 113–126

    Google Scholar 

  • Lynch M, Milligan BG (1994) Analysis of population genetic structure with RAPD markers. Mol Ecol 3:91–99

    Article  CAS  Google Scholar 

  • Mariette S, Le Corre V, Austerlitz F, Kremer A (2002) Sampling within the genome for measuring within-population diversity: trade-offs between markers. Mol Ecol 11:1145–1156

    Article  CAS  Google Scholar 

  • Martinez DE, Levinton J (1996) Adaptation to heavy metals in the aquatic oligochaete Limnodrilus hoffmeisteri: evidence for control by one gene. Evolution 50:1339–1343

    Article  Google Scholar 

  • McKenzie JA, Batterham P (1994) The genetic, molecular and phenotypic consequences of selection for insecticide resistance. Trends Ecol Evol 9:166–169

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Miller RG (1981) Simultaneous statistical inference, 2nd edn. Springer-Verlag Inc., New York

    Google Scholar 

  • Mitton JB (1997) Selection in natural populations. Oxford University Press, Oxford

    Google Scholar 

  • Moran MD (2003) Arguments for rejecting the sequential Bonferroni in ecological studies. Oikos 100:403–405

    Article  Google Scholar 

  • Mueller UG, Wolfenbarger LL (1999) AFLP genotyping and fingerprinting. Trends Ecol Evol 14:389–394

    Article  Google Scholar 

  • Mulvey M, Newman MC, Vogelbein WK, Unger MA (2002) Genetic structure of Fundulus heteroclitus from PAH-contaminated and neighboring sites in the Elizabeth and York Rivers. Aquat Toxicol 61:195–209

    Article  CAS  Google Scholar 

  • 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 22:671–677

    Article  CAS  Google Scholar 

  • Murdoch MH, Hebert PDN (1994) Mitochondrial DNA diversity of brown bullhead from contaminated and relatively pristine sites in the great lakes. Environ Toxicol Chem 13:1281–1289

    Article  CAS  Google Scholar 

  • Nacci DE, Coiro L, Champlin D, Jayaraman S, McKinney R, Gleason TR, Munns WR Jr, Specker JL, Cooper KR (1999) Adaptation of wild populations of the estuarine fish Fundulus heteroclitus to persistent environmental contaminants. Mar Biol 134:9–17

    Article  Google Scholar 

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

    Article  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

    Article  CAS  Google Scholar 

  • Nadig SG, Lee KL, Adams SM (1998) Evaluating alterations of genetic diversity in sunfish populations exposed to contaminants using RAPD assay. Aquat Toxicol 43:163–178

    Article  CAS  Google Scholar 

  • Nei M (1975) Molecular population genetics and evolution. North Holland Publishing Co., Amsterdam

    Google Scholar 

  • Nei M (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89:583–590

    Google Scholar 

  • Nelson WG, Bergen BJ, Benyi SJ, Morrison G, Voyer RA, Strobel CJ, Rego S, Thursby G, Pesch CE (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

  • Powers DA, Ropson I, Brown DC, Van Beneden R, Cashon R, Gonzalez-Villasenor LI, DiMichele JA (1986) Genetic variation in Fundulus heteroclitus: geographic distribution. Am Zool 26:131–144

    Google Scholar 

  • Pruell RJ, Norwood CB, Bowen RD, Boothman WS, Rogerson PF, Hackett M, Butterworth B (1990) Geochemical study of sediment contamination in New Bedford Harbor, Massachusetts. Mar Environ Res 29:77–101

    Article  CAS  Google Scholar 

  • 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 24:717–725

    Article  CAS  Google Scholar 

  • Safe S (1994) Polychlorinated biphenyls (PCBs): environmental impact, biochemical and toxic responses, and implications for risk assessment. Crit Rev Toxicol 24:87–149

    Article  CAS  Google Scholar 

  • Staton JL, Schizas NV, Chandler GT, Coull BC, Quattro JM (2001) Ecotoxicology and population genetics: the emergence of “phylogeographic and evolutionary toxicology”. Ecotoxicology 10:217–222

    Article  CAS  Google Scholar 

  • Street GT, Lotufo GR, Montagna PA, Fleeger JW (1998) Reduced genetic diversity in a meiobenthic copepod exposed to a xenobiotic. J Exp Mar Biol Ecol 222:93–111

    Article  CAS  Google Scholar 

  • Sweeney J, Deegan L, Garritt R (1998) Population size and site fidelity of Fundulus heteroclitus in a macrotidal saltmarsh creek. Biol Bull 195:238–239

    Article  Google Scholar 

  • Taylor MH, DiMichele L (1983) Spawning site utilization in a Delaware population of Fundulus heteroclitus (Pisces: Cyprinodontidae). Copeia 19:291–297

    Google Scholar 

  • Taylor M, Feyereisen R (1996) Molecular biology and evolution of resistance to toxicants. Mol Biol Evol 13:719–734

    CAS  Google Scholar 

  • Theodorakis CW (2001) Integration of genotoxic and population genetic endpoints in biomonitoring and risk assessment. Ecotoxicology 10:245–256

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Vos P, Hogers R, Bleeker M, Reijans M., van de Lee T, Hornes M, Frijters A, Pot J, Peleman J, Kuiper M, Zabeau M (1995) AFLP: a new technique for DNA fingerprinting. Nucleic Acids Res 23:4407–4414

    Article  CAS  Google Scholar 

  • Waples RS (1998) Separating the wheat from the chaff: patterns of genetic differentiation in high gene flow species. J Hered 89:438–450

    Article  Google Scholar 

  • Ward RD, Woodwark M, Skibinski DOF (1994) A comparison of genetic diversity levels in marine, freshwater, and anadromous fishes. J Fish Biol 44:213–227

    Article  Google Scholar 

  • Whitehead A, Anderson SL, Kuivila KM, Roach JL (2003) Genetic variation among interconnected populations of Catostomus occidentalis: implications for distinguishing impacts of contaminants from biogeographical structuring. Mol Ecol 12:2817–2833

    Article  CAS  Google Scholar 

  • Wright S (1943) Isolation by distance. Genetics 28:114–138

    CAS  Google Scholar 

  • Wright S (1978) Evolution and the genetics of populations. In: Variability within and among natural populations, Vol 4. University of Chicago Press, Chicago

    Google Scholar 

Download references

Acknowledgments

This work was performed while AM held a National Research Council Research Associateship. Statistical assistance and advisement was provided by A. Leonard, SoBran, and S. Franson, NERL, US EPA. Thanks to D. Champlin, NHEERL, US EPA for fish collections. Much appreciated reviews were provided by T. Gleason, J. Markert, and S. Roark and two anonymous reviewers. Special thanks to M. Duboise and S. Pelsue in the University of Southern Maine for providing workspace for some of this work.

Author information

Authors and Affiliations

  1. Biology Department, State University of New York College at Buffalo, 1300 Elmwood Ave., Buffalo, NY, 14222, USA

    Amy M. McMillan

  2. National Exposure Research Laboratory, Ecological Exposure Research Division, US EPA Office of Research and Development, Cincinnati, OH, USA

    Mark J. Bagley & Suzanne A. Jackson

  3. National Health and Environmental Effects Research Laboratory, Atlantic Ecology Division, US EPA Office of Research and Development, Narragansett, RI, USA

    Diane E. Nacci

Authors
  1. Amy M. McMillan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mark J. Bagley
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Suzanne A. Jackson
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Diane E. Nacci
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Amy M. McMillan.

Additional information

This is contribution number AED-05-096 of the US EPA ORD NHEERL Atlantic Ecology Division. Although the research described in this contribution has been funded partially by the US EPA, it has not been subjected to Agency-level review. Therefore, it does not necessarily reflect the views of the agency. Mention of trade names, products, or services does not constitute endorsement or recommendation for use.

Rights and permissions

Reprints and permissions

About this article

Cite this article

McMillan, A.M., Bagley, M.J., Jackson, S.A. et al. Genetic diversity and structure of an estuarine fish (Fundulus heteroclitus) indigenous to sites associated with a highly contaminated urban harbor. Ecotoxicology 15, 539–548 (2006). https://doi.org/10.1007/s10646-006-0090-4

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10646-006-0090-4

Keywords

Search

Navigation