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Genetic variation in strains of zebrafish (Danio rerio) and the implications for ecotoxicology studies

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Abstract

There is substantial evidence that genetic variation, at both the level of the individual and population, has a significant effect on behaviour, fitness and response to toxicants. Using DNA microsatellites, we examined the genetic variation in samples of several commonly used laboratory strains of zebrafish, Danio rerio, a model species in toxicological studies. We compared the genetic variation to that found in a sample of wild fish from Bangladesh. Our findings show that the wild fish were significantly more variable than the laboratory strains for several measures of genetic variability, including allelic richness and expected heterozygosity. This lack of variation should be given due consideration for any study which attempts to extrapolate the results of ecotoxicological laboratory tests to wild populations.

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References

  • Ankley GT, Johnson RD (2004) Small fish models for identifying and assessing the effects of endocrine-disrupting chemicals. ILAR J 45(4):469–483

    CAS  Google Scholar 

  • Armbruster P, Reed DH (2005) Inbreeding depression in benign and stressful environments. Heredity 95(3):235–242. doi:10.1038/sj.hdy.6800721

    Article  CAS  Google Scholar 

  • Athrey NRG, Leberg PL, Klerks PL (2007) Laboratory culturing and selection for increased resistance to cadmium reduced genetic variation in the least killifish, Heterandria formosa. Environ Toxicol Chem 26(9):1916–1921. doi:10.1897/06-589R.1

    Article  CAS  Google Scholar 

  • Barata C, Baird DJ, Amat F et al (2000) Comparing population response to contaminants between laboratory and field: an approach using Daphnia magna ephippial egg banks. Funct Ecol 14(4):513–523. doi:10.1046/j.1365-2435.2000.00445.x

    Article  Google Scholar 

  • Brown MCL, Guttman S, Glenn TC (2001) Development and use of microsatellite DNA loci for genetic ecotoxicological studies of the fathead minnow (Pimephales Promelas). Ecotoxicology 10(4):233–238. doi:10.1023/A:1016673528533

    Article  CAS  Google Scholar 

  • Bruford MW, Hanotte O, Brookfield JFY et al (1998) Multilocus and single-locus DNA fingerprinting. In: Hoelzel AR (ed) Molecular genetic analysis of populations: a practical approach, 2nd edn. IRL Press, Oxford

    Google Scholar 

  • Charpentier M, Setchell JM, Prugnolle F et al (2005) Genetic diversity and reproductive success in mandrills (Mandrillus sphinx). Proc Natl Acad Sci USA 102(46):16723–16728. doi:10.1073/pnas.0507205102

    Article  CAS  Google Scholar 

  • Chia R, Achilli F, Festing MFW et al (2005) The origins and uses of mouse outbred stocks. Nat Genet 37(11):1181–1186. doi:10.1038/ng1665

    Article  CAS  Google Scholar 

  • Chistiakov DA, Hellemans B, Volckaert FAM (2006) Microsatellites and their genomic distribution, evolution, function and applications: a review with special reference to fish genetics. Aquaculture 255(1–4):1–29. doi:10.1016/j.aquaculture.2005.11.031

    Article  CAS  Google Scholar 

  • Coe TS, Hamilton PB, Hodgson D et al (2008) An environmental estrogen alters reproductive hierarchies, disrupting sexual selection in group-spawning fish. Environ Sci Technol 42(13):5020–5025

    Article  CAS  Google Scholar 

  • David P (1998) Heterozygosity-fitness correlations: new perspectives on old problems. Heredity 80:531–537. doi:10.1046/j.1365-2540.1998.00393.x

    Article  Google Scholar 

  • Eisen JS (1996) Zebrafish make a big splash. Cell 87(6):969. doi:10.1016/S0092-8674(00)81792-4

    Article  CAS  Google Scholar 

  • Engeszer RE, Patterson LB, Rao AA et al (2007) Zebrafish in the wild: a review of natural history and new notes from the field. Zebrafish 4(1):21–40. doi:10.1089/zeb.2006.9997

    Article  Google Scholar 

  • Engeszer RE, Ryan MJ, Parichy DM (2004) Learned social preferences in zebrafish. Curr Biol 14:881–884. doi:10.1016/j.cub.2004.04.042

    Article  CAS  Google Scholar 

  • Felsenstein J (1995) Phylip (Phylogeny Inference Package). Department of Genetics, University of Washington, Seattle

    Google Scholar 

  • Fenske M, Maack G, Schafers C et al (2005) An environmentally relevant concentration of estrogen induces arrest of male gonad development in zebrafish, Danio rerio. Environ Toxicol Chem 24(5):1088–1098. doi:10.1897/04-096R1.1

    Article  CAS  Google Scholar 

  • Forbes VE (1998) Sources and implications of variability in sensitivity to chemicals for ecotoxicological risk assessment. Arch Toxicol Suppl 20:407–418

    CAS  Google Scholar 

  • Fritzsche P, Neumann K, Nasdal K et al (2006) Differences in reproductive success between laboratory and wild-derived golden hamsters (Mesocricetus auratus) as a consequence of inbreeding. Behav Ecol Sociobiol 60(2):220–226. doi:10.1007/s00265-006-0159-3

    Article  Google Scholar 

  • Gardeström J, Dahl U, Kotsalainen O et al (2008) Evidence of population genetic effects of long-term exposure to contaminated sediments—a multi-endpoint study with copepods. Aquat Toxicol 86(3):426–436. doi:10.1016/j.aquatox.2007.12.003

    Article  Google Scholar 

  • Gerhard GS, Cheng KC (2002) A call to fins! Zebrafish as a gerontological model. Aging Cell 1(2):104–111. doi:10.1046/j.1474-9728.2002.00012.x

    Article  CAS  Google Scholar 

  • Gerhard GS, Kauffman EJ, Wang XJ et al (2002) Life spans and senescent phenotypes in two strains of Zebrafish (Danio rerio). Exp Gerontol 37(8–9):1055–1068. doi:10.1016/S0531-5565(02)00088-8

    Article  Google Scholar 

  • Goudet J (1995) FSTAT (version 1.2): a computer program to calculate F-statistics. J Hered 86(6):485–486

    Google Scholar 

  • Gratton P, Allegrucci G, Gallozzi M et al (2004) Allozyme and microsatellite genetic variation in natural samples of zebrafish, Danio rerio. J Zoolog Syst Evol Res 42(1):54–62. doi:10.1046/j.0947-5745.2003.00240.x

    Article  Google Scholar 

  • Grunwald DJ, Eisen JS (2002) Timeline—Headwaters of the zebrafish emergence of a new model vertebrate. Nat Rev Genet 3(9):717–724. doi:10.1038/nrg892

    Article  CAS  Google Scholar 

  • Hansson B, Westerberg L (2002) On the correlation between heterozygosity and fitness in natural populations. Mol Ecol 11(12):2467–2474. doi:10.1046/j.1365-294X.2002.01644.x

    Article  Google Scholar 

  • Hill AJ, Teraoka H, Heideman W et al (2005) Zebrafish as a model vertebrate for investigating chemical toxicity. Toxicol Sci 86(1):6–19. doi:10.1093/toxsci/kfi110

    Article  CAS  Google Scholar 

  • Hoffman JI, Forcada J, Amos W (2006) No relationship between microsatellite variation and neonatal fitness in Antarctic fur seals, Arctocephalus gazella. Mol Ecol 15(7):1995–2005. doi:10.1111/j.1365-294X.2006.02894.x

    Article  CAS  Google Scholar 

  • Jeong D-S, Gonzalez EB, Morishima K et al (2007) Parentage assignment of stocked black sea bream Acanthopagrus schlegelii in Hiroshima Bay using microsatellite DNA markers. Fish Sci 73(4):823–830. doi:10.1111/j.1444-2906.2007.01402.x

    Article  CAS  Google Scholar 

  • Jones AG, Ardren WR (2003) Methods of parentage analysis in natural populations. Mol Ecol 12(10):2511–2523. doi:10.1046/j.1365-294X.2003.01928.x

    Article  CAS  Google Scholar 

  • Kretzmann M, Mentzer L, DiGiovanni R et al (2006) Microsatellite diversity and fitness in stranded juvenile harp seals (Phoca groenlandica). J Hered 97(6):555–560. doi:10.1093/jhered/esl043

    Article  CAS  Google Scholar 

  • Lieutenant-Gosselin M, Bernatchez L (2006) Local heterozygosity-fitness correlations with global positive effects on fitness in threespine stickleback. Evolution Int J Org Evolution 60(8):1658–1668

    CAS  Google Scholar 

  • Maack G, Segner H, Tyler CR (2003) Ontogeny of sexual differentiation in different strains of zebrafish (Danio rerio). Fish Physiol Biochem 28(1–4):125–128. doi:10.1023/B:FISH.0000030497.59378.88

    Article  CAS  Google Scholar 

  • Maes GE, Raeymaekers JAM, Pampoulie C et al (2005) The catadromous European eel Anguilla anguilla (L.) as a model for freshwater evolutionary ecotoxicology: relationship between heavy metal bioaccumulation, condition and genetic variability. Aquat Toxicol 73(1):99–114. doi:10.1016/j.aquatox.2005.01.010

    Article  CAS  Google Scholar 

  • McTavish K, Stech H, Stay F (1998) A modeling framework for exploring the population-level effects of endocrine disruptors. Environ Toxicol Chem 17(1):58–67. doi:10.1897/1551-5028(1998)017<0058:AMFFET>2.3.CO;2

    Article  CAS  Google Scholar 

  • Meng YB, Lin BL, Tominaga M et al (2006) Simulation of the population-level effects of 4-nonylphenol on wild Japanese medaka (Oryzias latipes). Ecol Modell 197(3–4):350–360. doi:10.1016/j.ecolmodel.2006.03.022

    Article  CAS  Google Scholar 

  • Miller DH, Ankley GT (2004) Modeling impacts on populations: fathead minnow (Pimephales promelas) exposure to the endocrine disruptor 17 beta-trenbolone as a case study. Ecotoxicol Environ Saf 59(1):1–9. doi:10.1016/j.ecoenv.2004.05.005

    Article  CAS  Google Scholar 

  • Minch E, Ruiz-Linares A, Goldstein D et al (1996) Microsat (version 1.5): a computer program for calculating various statistics on microsatellite allele data. http://hpgl.stanford.edu/projects/microsat/. Accessed 10 Sept 2008

  • Nash JP, Kime DE, Van der Ven LTM et al (2004) Long-term exposure to environmental concentrations of the pharmaceutical ethynylestradiol causes reproductive failure in fish. Environ Health Perspect 112(17):1725–1733

    CAS  Google Scholar 

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

    Google Scholar 

  • Nowak C, Jost D, Vogt C et al (2007) Consequences of inbreeding and reduced genetic variation on tolerance to cadmium stress in the midge Chironomus riparius. Aquat Toxicol 85(4):278–284

    CAS  Google Scholar 

  • Primmer CR, Landry PA, Ranta E et al (2003) Prediction of offspring fitness based on parental genetic diversity in endangered salmonid populations. J Fish Biol 63(4):909–927. doi:10.1046/j.1095-8649.2003.00200.x

    Article  Google Scholar 

  • Pujolar JM, Maes GE, Vancoillie C et al (2005) Growth rate correlates to individual heterozygosity in the European eel, Anguilla anguilla L. Evolution Int J Org Evolution 59(1):189–199

    CAS  Google Scholar 

  • Pujolar JM, Maes GE, Vancoillie C et al (2006) Environmental stress and life-stage dependence on the detection of heterozygosity-fitness correlations in the European eel, Anguilla anguilla. Genome 49(11):1428–1437. doi:10.1139/G06-104

    Article  CAS  Google Scholar 

  • Raymond M, Rousset F (1995) Genepop (version 1.2)—Population-genetics software for exact tests and ecumenicism. J Hered 86(3):248–249

    Google Scholar 

  • Reed DH, Frankham R (2003) Correlation between fitness and genetic diversity. Conserv Biol 17(1):230–237. doi:10.1046/j.1523-1739.2003.01236.x

    Article  Google Scholar 

  • Santos EM, Paull GC, Van Look KJW et al (2007) Gonadal transcriptome responses and physiological consequences of exposure to oestrogen in breeding zebrafish (Danio rerio). Aquat Toxicol 83(2):134. doi:10.1016/j.aquatox.2007.03.019

    Article  CAS  Google Scholar 

  • Shikano T, Taniguchi N (2002) Relationships between genetic variation measured by microsatellite DNA markers and a fitness-related trait in the guppy (Poecilia reticulata). Aquaculture 209(1–4):77–90. doi:10.1016/S0044-8486(01)00812-2

    Article  CAS  Google Scholar 

  • Slate J, David P, Dodds KG et al (2004) Understanding the relationship between the inbreeding coefficient and multilocus heterozygosity: theoretical expectations and empirical data. Heredity 93(3):255–265. doi:10.1038/sj.hdy.6800485

    Article  CAS  Google Scholar 

  • Spence R, Fatema MK, Reichard M et al (2006) The distribution and habitat preferences of the zebrafish in Bangladesh. J Fish Biol 69(5):1435–1448. doi:10.1111/j.1095-8649.2006.01206.x

    Article  Google Scholar 

  • Spence R, Smith C (2005) Male territoriality mediates density and sex ratio effects on oviposition in the zebrafish, Danio rerio. Anim Behav 69:1317–1323. doi:10.1016/j.anbehav.2004.10.010

    Article  Google Scholar 

  • Tiira K, Laurila A, Enberg K et al (2006a) Do dominants have higher heterozygosity? Social status and genetic variation in brown trout, Salmo trutta. Behav Ecol Sociobiol 59(5):657–665. doi:10.1007/s00265-005-0094-8

    Article  Google Scholar 

  • Tiira K, Laurila A, Peuhkuri N et al (2003) Aggressiveness is associated with genetic diversity in landlocked salmon (Salmo salar). Mol Ecol 12(9):2399–2407. doi:10.1046/j.1365-294X.2003.01925.x

    Article  Google Scholar 

  • Tiira K, Piironen J, Primmer CR (2006b) Evidence for reduced genetic variation in severely deformed juvenile salmonids. Can J Fish Aquat Sci 63(12):2700–2707. doi:10.1139/F06-154

    Article  Google Scholar 

  • Vilhunen S, Tiira K, Laurila A et al (2008) The bold and the variable: fish with high heterozygosity act recklessly in the vicinity of predators. Ethology 114(1):7–15

    Google Scholar 

  • Wang S, Hard JJ, Utter F (2002) Genetic variation and fitness in salmonids. Conserv Genet 3(3):321–333. doi:10.1023/A:1019925910992

    Article  CAS  Google Scholar 

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Acknowledgements

We thank Greg Paull for his assistance with fish husbandry and Jessica Miller from the University of Harvard for providing samples of zebrafish. Funded by the UK Environment Agency, Department of the Environment, Food and Rural Affairs, European Social Fund and University of Exeter to CRT and DH.

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Correspondence to C. R. Tyler.

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Coe, T.S., Hamilton, P.B., Griffiths, A.M. et al. Genetic variation in strains of zebrafish (Danio rerio) and the implications for ecotoxicology studies. Ecotoxicology 18, 144–150 (2009). https://doi.org/10.1007/s10646-008-0267-0

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