Skip to main content
Log in

Adaptive responses and latent costs of multigeneration cadmium exposure in parasite resistant and susceptible strains of a freshwater snail

  • Published:
Ecotoxicology Aims and scope Submit manuscript

Abstract

Population response to anthropogenic activities will be influenced by prior adaptation to environmental conditions. We tested how parasite-resistant and -susceptible strains of the freshwater snail, Biomphalaria glabrata, responded to cadmium and elevated temperature challenges after having been exposed to low-level cadmium continuously for multiple generations. Snails exposed to cadmium for three generations were removed for the fourth generation, and challenged in the fifth generation with (1) chronic cadmium exposure over the entire life cycle; (2) lethal cadmium exposure of adults; and (3) elevated temperature challenge of adults. The parasite susceptible NMRI strain is more cadmium tolerant than the parasite resistant BS90 strain and remained more tolerant than BS90 throughout this study. Additionally, NMRI exhibited greater adaptive capacity for cadmium than BS90 and became more tolerant of both chronic and lethal cadmium challenges, while BS90 became more tolerant of lethal cadmium challenge only. Fitness costs, reflected in population growth rate, were not apparent in fifth generation snails maintained in control conditions. However, costs were latent and expressed as decreased tolerance to a secondarily imposed temperature stress. Adaptation to prior selection pressures can influence subsequent adaptation to anthropogenic stresses and may have associated costs that reduce fitness in novel environments.

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

Access this article

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Antonovics J, Bradshaw AD, Turner RG (1971) Heavy metal tolerance in plants. Adv Ecol Res 7(1):85

    Google Scholar 

  • Bebianno MJ, Langston WJ (1995) Induction of metallothionein synthesis in the gill and kidney of Littorina littorea exposed to cadmium. J Mar Biol Ass UK 75:173–186

    Article  CAS  Google Scholar 

  • Carroll SP, Hendry AP, Reznick DN, Fox CW (2007) Evolution on ecological time-scales. Funct Ecol 21(3):387–393

    Article  Google Scholar 

  • Caswell H (2001) Matrix Population Models, 2nd edn. Sinauer Associates, Sunderland

    Google Scholar 

  • Cook SheilaCA, Lefébvre Claude, McNeilly Thomas (1971) Competition betwen metal tolerant and normal plant populations on normal soil. Evolution 26:366–372

    Article  Google Scholar 

  • Coustau C, Chevillon C, ffrench-Constant. R (2000) Resistance to xenobiotics and parasites: can we count the cost? Trends Ecol Evol 15(9):378–383

    Article  Google Scholar 

  • Dallinger R, Janssen HH, Bauer-Hilty A, Berger B (1989) Characterization of an inducible cadmium-binding protein from the hepatopancreas of metal-exposed slugs (Arionidae, Mollusca). Comp Biochem Physiol C 92C(2):355–360

    Article  CAS  Google Scholar 

  • Ebert, Thomas A (1999) Plant and Animal Populatons: Methods in Demography. Academic Press, San Diego

    Google Scholar 

  • Guan R, Wang WX (2006) Comparison between two clones of Daphnia magna: Effects of multigenerational cadmium exposure on toxicity, individual fitness, and biokinetics. Aquat Toxicol 76:217–229

    Article  CAS  Google Scholar 

  • Hairston NG, Ellner SP, Geber MA, Yoshida T, Fox JA (2005) Rapid evolution and the convergence of ecological and evolutionary time. Ecol Lett 8(10):1114–1127

    Article  Google Scholar 

  • Hickey DA, McNeilly T (1974) Competition between metal tolerant and normal plant populations: a field experiment on normal soil. Evolution 29:458–464

    Article  Google Scholar 

  • Janssen CR, De Schamphelaere K, Heijerick D, Muyssen B, Lock K, Bossuyt B, Vangheluwe M, Van Sprang P (2000) Uncertainties in the environmental risk assessment of metals. Hum Ecol Risk Assess 6(6):1003–1018

    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 

  • Langand J, Jourdane J, Coustau C, Delay B, Morand S (1998) Cost of resistance, expressed as delayed maturity, detected in the host-parasite system Biomphalaria glabrata/Echinostoma caproni. Heredity 80:320–325

    Article  Google Scholar 

  • Lewis FA, Patterson CN, Grzywacz C (2003) Parasite-susceptibility phenotypes of F 1 Biomphalaria glabrata progeny derived from interbreeding Schistosoma mansoni-resistant and-susceptible snails. Parasitol Res 89(2):98–101

    Article  Google Scholar 

  • Lin HC, Hsu SC, Hwang PP (2000) Maternal transfer of cadmium tolerance in larval Oreochromis mossambicus. J Fish Biol 57(1):239–248

    Article  CAS  Google Scholar 

  • Macnair MR (1991) Why the evolution of resistance to anthropogenic toxins normally involves major gene changes: the limits to natural selection. Genetica 84:213–219

    Article  Google Scholar 

  • Maroni G, Wise J, Young JE, Otto E (1987) Metallothionein gene duplications and metal tolerance in natural populations of Drosophila melanogaster. Genetics 117:739–744

    CAS  Google Scholar 

  • McGraw JB, Caswell H (1996) Estimation of Individual Fitness from Life-History Data. Am Nat 147(1):47

    Article  Google Scholar 

  • Meyer JN, Di Giulio RT (2003) Heritablew adaptation and fitness costs in killifish (Fundulus heteroclitus) inhabiting a polluted estuary. Ecol Appl 13(2):490–503

    Article  Google Scholar 

  • Mulvey M, Diamond S (1990) Genetic factors and tolerance acquisition in populations exposed to metals and metalloids. In: Newman MC, McIntosh AW (eds) Metal ecotoxicolgy, concepts and applications. Lewis Publishers, Orlando, FL

    Google Scholar 

  • Muyssen BTA, Janssen CR (2004) Multi-generation cadmium acclimation and tolerance in Daphnia magna Straus. Environ Pollut 130:309–316

    Article  CAS  Google Scholar 

  • Nacci D, Coiro L, Champlin D, Jayaraman S, McKinney R, Gleason TR, Munns WR Jr, Specker JL, Cooper KR (1999) Adaptations of wild populations of the estuarine fish Fundulus heteroclitus to persistent environmental contaminants. Mar Biol 134(1):9–17

    Article  Google Scholar 

  • Newman MC, Dixon PM (1996) Ecologically meaningful estimates of lethal effect in individuals. In: Newman MC, Jagoe CH (eds) Ecotoxicology: A hierarchical treatment. CRC Press, Boca Raton, FL

    Google Scholar 

  • Palumbi SR (2001) Humans as the world’s greatest evolutionary force. Science 293(5536):1786–1790

    Article  CAS  Google Scholar 

  • 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 106c(1):11–38

    CAS  Google Scholar 

  • Postma JF, van Kleunen A, Admiraal W (1995a) Alterations in life-history traits of Chironomus riparius (Diptera) obtained from metal contaminated rivers. Arch Environ Contam Toxicol 29:469–475

    Article  CAS  Google Scholar 

  • Postma JF, Mol S, Larsen H, Admiraal W (1995b) Life-cycle changes and zinc shortage in cadmium-tolerant midges, Chironomus riparius (Diptera), reared in the absence of cadmium. Environ Toxicol Chem 14(1):117–122

    CAS  Google Scholar 

  • Postma JF, van Nugteren P, Buckert-De Jong MB (1996) Increased cadmium excretion in metal-adapted populations of the midge Chironomus riparius (Diptera). Environ Toxicol Chem 15(3):332–339

    CAS  Google Scholar 

  • Raymond B, Sayyed AH, Wright DJ (2005) Genes and environment interact to determine the fitness costs of resistance to Bacillus thuringiensis. Proc R Soc B: Biol Sci 272(1571):1519–1524

    Article  CAS  Google Scholar 

  • Roesijadi G (1992) Metallothioneins in metal regulation and toxicity in aquatic animals. Aquat Toxicol 22:81–114

    Article  CAS  Google Scholar 

  • Roff DA, Fairbairn DJ (2007) The evolution of trade-offs: where are we? J Evol Biol 20(2):433

    Article  CAS  Google Scholar 

  • Roush RT, McKenzie JA (1987) Ecological genetics of insecticide and acaricide resistance. Annu Rev Entomol 32(1):361–380

    Article  CAS  Google Scholar 

  • Salice CJ, Miller TJ (2003) Population-level responses to long-term cadmium exposure in two strains for the freshwater gastropod, Biomphalaria glabrata: Results from a life-table response experiment. Environ Toxicol Chem 22(3):678–688

    CAS  Google Scholar 

  • Salice CJ, Miller TJ and Roesijadi G (2009) Demographic Responses to Multigeneration Cadmium Exposure in Two Strains of the Freshwater Gastropod, Biomphalaria glabrata. Arch Environ Contam Toxicol 56(4):785–795

    Article  CAS  Google Scholar 

  • Salice CJ, Christopher J, Roesijadi G (2002) Resistance to cadmium and parasite infection are inversely related in two strains of a freshwater gastropod. Environ Toxicol Chem 21(7):1398–1403

    Article  CAS  Google Scholar 

  • Sgrò CM, Hoffmann AA (2004) Genetic correlations, tradeoffs and environmental variation. Heredity 93:241–248

    Article  Google Scholar 

  • Shirley MDF, Sibly RM (1999) Genetic basis of a between-environment trade-off involving resistance to cadmium in Drosophila melanogaster. Evolution 53(3):826–836

    Article  Google Scholar 

  • R Development Core Team (2006) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL http://www.R-project.org

  • Thompson JN (1998) Rapid evolution as an ecological process. Trends Ecol Evol 13(8):329–332

    Article  Google Scholar 

  • Ward TJ, Robinson WE (2005) Evolution of cadmium resistance in Daphnia magna. Environ Toxicol Chem 24(9):2341–2349

    Article  CAS  Google Scholar 

  • Webster JP, and MEJ Woolhouse (1999) Cost of resistance: relationship between reduced fertility and increased resistance in a snail-schistosome host-parasite system. Proc: Biol Sci 266(1417):391-396

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Xie L, Klerks PL (2003) Responses to selection for cadmium resistance in the least killifish, Heterandria formosa. Environ Toxicol Chem 22(2):313–320

    CAS  Google Scholar 

  • Xie L, Klerks PL (2004a) Changes in cadmium accumulation as a mechanism for cadmium resistance in the least killifish Heterandria formosa. Aquat Toxicol 66(1):73–81

    Article  CAS  Google Scholar 

  • Xie L, Klerks PL (2004b) Fitness costs of resistance to cadmium in the least killifish (Heterandria formosa). Environ Toxicol Chem 23(6):1499–1503

    Article  CAS  Google Scholar 

  • Yoshida T, Jones LE, Ellner SP, Fussmann GF, Hairston NG (2003) Rapid evolution drives ecological dynamics in a predator–prey system. Nature 424(6946):303–306

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We would like to thank David Rogowski, Jonathan Maul and two anonymous reviewers for providing constructive comments on previous drafts of the manuscript. Support from the following organizations is acknowledged: NIH Training Grant T32 ES-7263 to the Program in Toxicology, University of Maryland, Baltimore, and the Graduate Student Association, University of Maryland, Baltimore. Fred Lewis of the Biomedical Research Institute kindly provided snails and husbandry advice. This study was conducted at the University of Maryland Center for Environmental Science, Chesapeake Biological Laboratory.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Christopher J. Salice.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Salice, C.J., Anderson, T.A. & Roesijadi, G. Adaptive responses and latent costs of multigeneration cadmium exposure in parasite resistant and susceptible strains of a freshwater snail. Ecotoxicology 19, 1466–1475 (2010). https://doi.org/10.1007/s10646-010-0532-x

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10646-010-0532-x

Keywords

Navigation