, Volume 22, Issue 5, pp 929–937 | Cite as

Differential tolerance to copper, but no evidence of population-level genetic differences in a widely-dispersing native barnacle

  • Mailie L. Gall
  • Sebastian P. Holmes
  • Katherine A. Dafforn
  • Emma L. Johnston


Despite many estuaries having high levels of metal pollution, species are found to persist in these stressful environments. Populations of estuarine invertebrates exposed to toxic concentrations of such metals may be under selection. However, in species with a wide-dispersal potential, any short-term results of localized selection may be counteracted by external recruitment from populations not under selection. The barnacle Amphibalanus variegatus is found in nearshore coastal environments as well as sheltered embayments and estuaries, including metal-impacted estuaries, from New South Wales, Australia to Western Australia. The fertilised eggs of A. variegatus are brooded internally and released as larvae (nauplii), which remain in the water-column for ~14 days before settling. Hence the species has a considerable dispersal capacity. The purpose of this study was to examine whether populations of A. variegatus from metal-impacted sites, displayed a greater tolerance to a toxicant (copper) than reference populations. Adult barnacles where collected from twenty sites within two metal-impacted and fourteen sites within two reference estuaries. Within 24 h, adults were induced to spawn and the offspring were exposed to copper in a laboratory assay. Larvae collected from the metal-impacted estuaries demonstrated a greater tolerance to copper compared to those from reference sites. To determine if selection/localised in the metal impacted sites was occurring, the genetic structure of populations at three sites was examined using an AFLP methodology. No evidence of unique population identity and or selection (outlier loci) was detected suggesting that: (1) the tolerance displayed in the assay was derived from acclimation during development; and/or (2) that the populations are open preventing the fixation of any unique alleles.


Tolerance Acclimation Selection Copper AFLP 



We would like to thank members of the Subtidal Ecology and Ecotoxicology laboratory and volunteers for their assistance. This Project was supported by an Australian Research Council Grant awarded to Johnston EL and Doyle C.


  1. Barton N, Partridge L (2000) Limits to natural selection. Bioessays 22(12):1075–1084CrossRefGoogle Scholar
  2. Belfiore NM, Anderson SL (2001) Effects of contaminants on genetic patterns in aquatic organisms: a review. Mutat Res 489(2–3):97–122Google Scholar
  3. Birch GF (1996) Sediment-bound metallic contaminants in Sydney’s estuaries and adjacent offshore, Australia. Estuar Coast Shelf Sci 42(1):31–44CrossRefGoogle Scholar
  4. Birch GF, Evenden D, Teutsch ME (1996) Dominance of point source in heavy metal distributions in sediments of a major Sydney estuary (Australia). Environ Geol 28(4):169–174CrossRefGoogle Scholar
  5. Bryan GW, Langston WJ (1992) Bioavailability, accumulation and effects of heavy metals in sediments with special reference to United Kingdom estuaries: a review. Environ Pollut 76(2):89–131CrossRefGoogle Scholar
  6. Caley MJ, Carr MH, Hixon MA, Hughes TP, Jones GP, Menge BA (1996) Recruitment and the local dynamics of open marine populations. Annu Rev Ecol Syst 27:477–500CrossRefGoogle Scholar
  7. Campbell D, Bernatchez L (2004) Generic scan using AFLP markers as a means to assess the role of directional selection in the divergence of sympatric whitefish ecotypes. Mol Biol Evol 21(5):945–956CrossRefGoogle Scholar
  8. Chapman GA (1985) Acclimation as a factor influencing metal criteria. In: Bahner RC, Hansen DJ (eds) Aquatic toxicology and hazard assessment: eighth symposium. American Society for Testing Metals, Philadelphia, 1985, pp 119–136Google Scholar
  9. Clarke LM, Munch SB, Thorrold SR, Conover DO (2010) High connectivity among locally adapted populations of a marine fish (Menidia menidia). Ecology 91(12):3526–3537CrossRefGoogle Scholar
  10. Coors A, Vanoverbeke J, De Bie T, De Meester L (2009) Land use, genetic diversity and toxicant tolerance in natural populations of Daphnia magna. Aquat Toxicol 95(1):71–79CrossRefGoogle Scholar
  11. Cowen RK, Sponaugle S (2009) Larval dispersal and marine population connectivity. In: Annual Review of Marine Science, vol 1. Annual Reviews, Palo Alto, pp 443–466Google Scholar
  12. Dafforn KA, Glasby TM, Johnston EL (2009) Links between estuarine condition and spatial distributions of marine invaders. Divers Distrib 15(5):807–821CrossRefGoogle Scholar
  13. Dafforn KA, Simpson SL, Kelaher BP, Clark GF, Komyakova V, Wong CKC, Johnston EL (2012) The challenge of choosing environmental indicators of anthropogenic impacts in estuaries. Environ Pollut 163:207–217CrossRefGoogle Scholar
  14. Depledge MH (1994) Genotypic toxicity: implications for individuals and populations. Environ Health Perspect 102:101–104CrossRefGoogle Scholar
  15. DLWC (2000) Estuaries of New South Wales. Sydney, Australia: Department of Land and Water ConservationGoogle Scholar
  16. Egan EA, Anderson DT (1986) Larval development of Balanus amphitrite Darwin and Balanus variegatus Darwin (Cirripedia, Balanidae) from New South Wales, Australia. Crustaceana 51(2):188–207CrossRefGoogle Scholar
  17. Evenden D: Heavy metal concentrations in the sediments of the Georges River, N. S. W. unpublished honours thesis (1992)Google Scholar
  18. Fischer MC, Foll M, Excoffier L, Heckel G (2011) Enhanced AFLP genome scans detect local adaptation in high-altitude populations of a small rodent (Microtus arvalis). Mol Ecol 20(7):1450–1462CrossRefGoogle Scholar
  19. Fisher M, Oleksiak M (2007) Convergence and divergence in gene expression among natural populations exposed to pollution. BMC Genomics 8(1):108CrossRefGoogle Scholar
  20. Foll M, Gaggiotti O (2008) A genome-scan method to identify selected loci appropriate for both dominant and codominant markers: a bayesian perspective. Genetics 180(2):977–993CrossRefGoogle Scholar
  21. Fritsch C, Coeurdassier M, Gimbert F, Crini N, Scheifler R, Vaufleury A (2011) Investigations of responses to metal pollution in land snail populations (Cantareus aspersus and Cepaea nemoralis) from a smelter-impacted area. Ecotoxicology 20(4):739–759CrossRefGoogle Scholar
  22. Gall ML, Poore AGB, Johnston EL (2012) A biomonitor reflects an ecologically-significant fraction of metals in an industrialised harbour. J Environ Monitor 14(3):830–838CrossRefGoogle Scholar
  23. García-Ramos G, Kirkpatrick M (1997) Genetic models of adaptation and gene flow in peripheral populations. Evolution 51(1):21–28CrossRefGoogle Scholar
  24. Grant A (2002) Pollution-tolerant species and communities: intriguing toys or invaluable monitoring tools? Hum Ecol Risk Assess 8(5):955–970CrossRefGoogle Scholar
  25. Grant A, Hateley JG, Jones NV (1989) Mapping the ecological impact of heavy metals on the estuarine polychaete Nereis diversicolor using inherited metal tolerance. Mar Pollut Bull 20(5):235–238CrossRefGoogle Scholar
  26. Groenendijk D, Lucker SMG, Plans M, Kraak MHS, Admiraal W (2002) Dynamics of metal adaptation in riverine chironomids. Environ Pollut 117(1):101–109CrossRefGoogle Scholar
  27. Hayes WJ, Anderson IJ, Gaffoor MZ, Hurtado J (1998) Trace metals in oysters and sediments of Botany Bay, Sydney. Sci Total Environ 212(1):39–47CrossRefGoogle Scholar
  28. He ZJ, Morrison RJ (2001) Changes in the marine environment of Port Kembla Harbour, NSW, Australia, 1975–1995: a review. Mar Pollut Bull 42(3):193–201CrossRefGoogle Scholar
  29. Hillis DM, Mable BK, Larson A, Davis SK, Zimmer EA (1996) Nucleic acids IV: sequencing and cloning. In: Hillis DM, Moritz C, Mable BK (eds) Molecular systematics, 2nd edn. Sinauer Asssociates Inc., MassachusettsGoogle Scholar
  30. Johnston EL (2011) Tolerance to contaminants: evidence from chronically exposed populations of aquatic organisms. In: Romeo M, Rainbow PS, Amiard-Triquet C (eds) Tolerance to environmental contaminants. CRC Press, Boca Raton, pp 25–46CrossRefGoogle Scholar
  31. Kawecki TJ, Ebert D (2004) Conceptual issues in local adaptation. Ecol Lett 7(12):1225–1241CrossRefGoogle Scholar
  32. Klerks P (1999) Acclimation to contaminants by the grass shrimp Palaemonetes pugio: individual contaminants vs. mixtures. Ecotoxicology 8(4):277–286CrossRefGoogle Scholar
  33. Klerks P, Lentz S (1998) Resistance to lead and zinc in the western mosquitofish Gambusia affinis inhabiting contaminated Bayou Trepagnier. Ecotoxicology 7(1):11–17CrossRefGoogle Scholar
  34. Klerks PL, Levinton JS (1989) Rapid evolution of metal resistance in a benthic oligochaete inhabiting a metal-polluted site. Biol Bull 176(2):135–141CrossRefGoogle Scholar
  35. Klerks PL, Moreau CJ (2001) Heritability of resistance to individual contaminants and to contaminant mixtures in the sheepshead minnow (Cyprinodon variegatus). Environ Toxicol Chem 20(8):1746–1751Google Scholar
  36. Klerks PL, Weis JS (1987) Genetic adaptation to heavy metals in aquatic organisms: a review. Environ Pollut 45(3):173–205CrossRefGoogle Scholar
  37. Lenormand T (2002) Gene flow and the limits to natural selection. Trends in ecology & evolution (Personal edition) 17(4):183–189CrossRefGoogle Scholar
  38. Lopes I, Baird DJ, Ribeiro R (2004) Genetic determination of tolerance to lethal and sublethal copper concentrations in field populations of Daphnia longispina. Arch Environ Contam Toxicol 46:43–51CrossRefGoogle Scholar
  39. Medina MH, Correa JA, Barata C (2007) Micro-evolution due to pollution: possible consequences for ecosystem responses to toxic stress. Chemosphere 67(11):2105–2114CrossRefGoogle Scholar
  40. Meyer JN, Giulio RTD (2003) Heritable adaptation and fitness costs in killifish (Fundulus heteroclitus) inhabiting a polluted estuary. Ecol Appl 13(2):490–503CrossRefGoogle Scholar
  41. Miliou H, Verriopoulos G, Maroulis D, Bouloukos D, Moraitou-apostolopoulou M (2000) Influence of life-history adaptations on the fidelity of laboratory bioassays for the impact of heavy metals (Co2+ and Cr6+) on tolerance and population dynamics of Tisbe holothuriae. Mar Pollut Bull 40(4):352–359CrossRefGoogle Scholar
  42. Millward RN, Klerks PL (2002) Contaminant-adaptation and community tolerance in ecological risk assessment: introduction. Hum Ecol Risk Assess 8(5):921–932CrossRefGoogle Scholar
  43. Moran PJ (1984) Water-quality control and its effect on the concentration of heavy-metals in Port-Kembla Harbor, NSW. Mar Pollut Bull 15(8):294–297CrossRefGoogle Scholar
  44. Morgan AJ, Kille P, Stürzenbaum SR (2007) Microevolution and ecotoxicology of metals in invertebrates. Environ Sci Technol 41(4):1085–1096CrossRefGoogle Scholar
  45. Münzinger A, Monicelli F (1992) Heavy metal co-tolerance in a chromium tolerant strain of Daphnia magna. Aquat Toxicol 23(3–4):203–216CrossRefGoogle Scholar
  46. Palumbi SR (1994) Genetic divergence, reproductive isolation, and marine speciation. Annu Rev Ecol Syst 25:547–572CrossRefGoogle Scholar
  47. Peakall ROD, Smouse PE (2006) Genalex 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6(1):288–295CrossRefGoogle Scholar
  48. Piola RF, Johnston EL (2008) Pollution reduces native diversity and increases invader dominance in marine hard-substrate communities. Divers Distrib 14(2):329–342CrossRefGoogle Scholar
  49. Posthuma L, Van Straalen NM (1993) Heavy-metal adaptation in terrestrial invertebrates: a review of occurrence, genetics, physiology and ecological consequences. Comp Biochem Physiol C 106(1):11–38Google Scholar
  50. Qiu J-W, Thiyagarajan V, Cheung S, Qian P-Y (2005) Toxic effects of copper on larval development of the barnacle Balanus amphitrite. Mar Pollut Bull 51(8–12):688–693CrossRefGoogle Scholar
  51. Rainbow PS, Amiard-Triquet C, Amiard JC, Smith BD, Best SL, Nassiri Y, Langston WJ (1999) Trace metal uptake rates in crustaceans (amphipods and crabs) from coastal sites in NW Europe differentially enriched with trace metals. Mar Ecol Prog Ser 183:189–203CrossRefGoogle Scholar
  52. Romano JA, Rittschof D, McClellan-Green PD, Holm ER (2010) Variation in toxicity of copper pyrithione among populations and families of the barnacle, Balanus amphitrite. Biofouling 26(3):341–347CrossRefGoogle Scholar
  53. Sanford E, Kelly MW (2011) Local adaptation in marine invertebrates. Annu rev marine sci 3(1):509–535CrossRefGoogle Scholar
  54. Sarkar A, Ray D, Shrivastava A, Sarker S (2006) Molecular biomarkers: their significance and application in marine pollution monitoring. Ecotoxicology 15(4):333–340CrossRefGoogle Scholar
  55. Scanes PR, Roach AC (1999) Determining natural ‘background’ concentrations of trace metals in oysters from New South Wales, Australia. Environ Pollut 105(3):437–446CrossRefGoogle Scholar
  56. Slatkin M (1987) Gene flow and the geographic structure of natural populations. Science 236(4803):787–792CrossRefGoogle Scholar
  57. Sotka EE (2005) Local adaptation in host use among marine invertebrates. Ecol Lett 8(4):448–459CrossRefGoogle Scholar
  58. Spooner DR, Maher W, Otway N (2003) Trace metal concentrations in sediments and oysters of Botany Bay, NSW, Australia. Arch Environ Contam Toxicol 45(1):92–101CrossRefGoogle Scholar
  59. Stapley J, Reger J, Feulner PGD, Smadja C, Galindo J, Ekblom R, Bennison C, Ball AD, Beckerman AP, Slate J (2010) Adaptation genomics: the next generation. Trends Ecol Evol 25(12):705–712CrossRefGoogle Scholar
  60. Teutsch ME: The distribution of heavy metals in Botany Bay and the lower Georges River, N.S.W. unpublished honours thesis, University of Sydney (1992)Google Scholar
  61. Untersee S, Pechenik JA (2007) Local adaptation and maternal effects in two species of marine gastropod (genus Crepidula) that differ in dispersal potential. Mar Ecol Prog Ser 347:79–85CrossRefGoogle Scholar
  62. Van Straalen NM, Janssens TS, Roelofs D (2011) Micro-evolution of toxicant tolerance: from single genes to the genome’s tangled bank. Ecotoxicology 20(3):574–579CrossRefGoogle Scholar
  63. Vos P, Hogers R, Bleeker M, Reijans M, Lee Tvd, Hornes M, Friters A, Pot J, Paleman J, Kuiper M, Zabeau M (1995) AFLP: a new technique for DNA fingerprinting. Nucleic Acids Res 23(21):4407–4414CrossRefGoogle Scholar
  64. Wang W-X, Rainbow PS (2005) Influence of metal exposure history on trace metal uptake and accumulation by marine invertebrates. Ecotoxicol Environ Saf 61(2):145–159CrossRefGoogle Scholar
  65. Wang T, Chen G, Zan Q, Wang C, Su Y-j (2012) AFLP genome scan to detect genetic structure and candidate loci under selection for local adaptation of the invasive weed Mikania micrantha. PLoS One 7(7):e41310CrossRefGoogle Scholar
  66. Williams LM, Oleksiak MF (2008) Signatures of selection in natural populations adapted to chronic pollution. BMC Evol Biol 8(1):282CrossRefGoogle Scholar
  67. Wirgin I, Waldman JR (2004) Resistance to contaminants in North American fish populations. Mutat Res 552(1–2):73–100Google Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  • Mailie L. Gall
    • 1
    • 2
  • Sebastian P. Holmes
    • 2
    • 3
  • Katherine A. Dafforn
    • 1
  • Emma L. Johnston
    • 1
  1. 1.Evolution and Ecology Research Centre, School of Biological, Earth and Environmental SciencesUniversity of New South WalesSydneyAustralia
  2. 2.Water and Wildlife Ecology Group, School of Science and HealthUniversity of Western SydneyPenrithAustralia
  3. 3.School of Biological SciencesUniversity of SydneySydneyAustralia

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