Behavior Genetics

, 36:271 | Cite as

QTL Analysis of Behavioral and Morphological Differentiation Between Wild and Laboratory Zebrafish (Danio rerio)

  • Dominic Wright
  • Reiichiro Nakamichi
  • Jens Krause
  • Roger K. Butlin
Article

The zebrafish is an important model organism for neuro-anatomy and developmental genetics. It also offers opportunities for investigating the functional and evolutionary genetics of behaviour but these have yet to be exploited. The ecology of anti-predator behaviour has been widely studied in fish and has been shown to vary among populations and between wild and domesticated (laboratory) fish. Here, we utilise the strong behavioural differences present between a wild-derived strain of fish from Bangladesh and the laboratory strain AB. In total, 184 F2 fish were generated and tested for shoaling tendency and willingness to approach an unfamiliar object (‘boldness’). Our results indicate the existence of QTL for boldness on chromosomes 9 and 16 and suggest another genomic region that influences anti-predator behaviour on chromosome 21. QTL for growth rate, weight and fat content, all of which are elevated in laboratory fish, were detected on chromosome 23. These initial results confirm the potential for QTL mapping of behavioural traits in zebrafish and also for dissecting the consequences of selection during domestication.

Keywords

Anxiety boldness domestication growth QTL shoaling zebrafish 

References

  1. Akaike H. (1974). A new look at the statistical model identification. IEEE Trans. Autom. Contr. AC-19:716–723CrossRefGoogle Scholar
  2. Baird T. A., Ryer C. H., Olla B. L. (1991). Social enhancement of foraging on an ephemeral food source in juvenile Wall-eye Pollock, Theragra chalcogramma. Environ. Biol. Fishes 31:307–311CrossRefGoogle Scholar
  3. Berejikian B. A. (1995). The effects of hatchery and wild ancestry and experience on the relative ability of steelhead trout fry (Oncorhynchus mykiss) to avoid a benthic predator. Can. J. Fish. Aquat. Sci. 52:2476–2482CrossRefGoogle Scholar
  4. Berejikian B. A., Mathews S. B., Quinn T. P. (1996). Effects of hatchery and wild ancestry and rearing environments on the development of agonistic behaviour in steelhead trout (Oncorhynchus mykiss) fry. Can. J. Fish. Aquat. Sci. 53:2004–2014CrossRefGoogle Scholar
  5. Budaev S. V. (1997). Personality in the guppy (Poecilia reticluata) : A correlational study of exploratory behaviour and social tendency. J. Comp. Psych. 111:399–411CrossRefGoogle Scholar
  6. Budaev S. V., Zhuikov A. Y. (1998). Avoidance learning and personality in the guppy (Poecilia reticulata). J. Comp. Psych. 112:92–94CrossRefGoogle Scholar
  7. Carlborg Ö., Kerje S., Schutz K., Jacobsson L., Jensen P., Andersson L. (2003). A global search revals epistatic interaction between QTL for early growth in the chicken. Genome Res. 13:413–421PubMedCrossRefGoogle Scholar
  8. Churchill G. A., Doerge R. W. (1994). Empirical threshold values for quantitative trait mapping. Genetics 138:964–971Google Scholar
  9. Coleman K., Wilson D. S. (1998). Shyness and boldness in pumpkinseed sunfish: Individual differences are context-specific. Anim. Behav. 56:927–936PubMedCrossRefGoogle Scholar
  10. Csanyi V. (1985). Ethological analysis of predator avoidance by the paradise fish (Macropodus opercularis L.) I. Recognition and learning of predators. Behaviour 92:227–240Google Scholar
  11. Darvasi A. (1998). Experimental strategies for the genetic dissection of complex traits in animal models. Nat. Genet. 18:19–24PubMedCrossRefGoogle Scholar
  12. de Bono M., Bargmann C. I. (1998). Natural variation in a neuropeptide Y receptor homolog modifies social behavior and food response in C. elegans. Cell 94:679–689PubMedCrossRefGoogle Scholar
  13. DeFries J. C., Gervais M. C., Thomas E. A. (1978). Response to 30 generations of selection for open field activity in laboratory mice. Behav. Genet. 8:3–13PubMedCrossRefGoogle Scholar
  14. deVicente M. C., Tanksley S. D. (1993). QTL Analysis of transgressive segregation in an interspecific tomato cross. Genetics 134:585–596PubMedGoogle Scholar
  15. Doerge R. W., Churchill G. A. (1996). Permutation tests for multiple loci affecting a quantitative character. Genetics 142:285–294PubMedGoogle Scholar
  16. Falconer, D. S. and Mackay, T. F. C. (1996). Introduction to quantitative genetics. Prentice HallGoogle Scholar
  17. Fleming I. A., Einum S. (1997). Experimental tests of genetic divergence of farmed from wild atlantic Salmon due to domestication. ICES J. Marine Sci. 54:1051–1063Google Scholar
  18. Flint J. (2003). Analysis of quantitative trait loci that influence animal behaviour. J. Neurobiol. 54:46–77PubMedCrossRefGoogle Scholar
  19. Flint J., Corley J. C., DeFries J. C., Fulker D. W., Gray J. A., Miller S., Collins A. C. (1995). A simple genetic basis for a complex psychological trait in laboratory mice. Science 269:1432–1435PubMedCrossRefGoogle Scholar
  20. Gjedrem T. (2000). Genetic improvement of cold-water fish species. Aquac. Res. 31(1):25–35CrossRefGoogle Scholar
  21. Hall C. S. (1951). The genetics of behavior handbook of experimental psychology. S. S. Stevens. New York, WileyGoogle Scholar
  22. Henderson N. D., Turri M. G., DeFries J. C., Flint J. (2004). QTL analysis of multiple behavioral measures of anxiety in mice. Behav. Genet. 34:267–293PubMedCrossRefGoogle Scholar
  23. Johnsson J., Petersson E., Jonsson E., Bjornsson B., Jarvi T. (1996). Domestication and growth hormone alter antipredator behaviour and growth patterns in juvenile brown trout, Salmo trutta. Can. J. Fish. Aquat. Sci. 53:1546–1554CrossRefGoogle Scholar
  24. Johnsson J. I., Abrahams M. V. (1991). Interbreeding with domestic strain increases foraging under threat of predation in juvenile steelhead trout (Oncorhynchus mykiss): An experimental study. Can. J. Fish. Aquat. Sci. 48:243–247CrossRefGoogle Scholar
  25. Koide T., Moriwaka K., Ikeda K., Niki H., Shiroishi T. (2000). Multi-phenotype behavioral characterization of inbred strains derived from wild stocks of Mus musculus. Mamm. Gen. 11:664–670CrossRefGoogle Scholar
  26. Krause J., Ruxton G. (2002). Living In Groups. Oxford, Oxford University PressGoogle Scholar
  27. Landeau L., Terborgh J. (1986). Oddity and the confusion effect in predation. Anim. Behav. 34:1372–1380CrossRefGoogle Scholar
  28. Lander E.S., Botstein D. (1989). Mapping Mendelian factors underlying quantitative traits using RFLP linkage maps. Genetics 121:185–199PubMedGoogle Scholar
  29. Lander E., Kruglyak L. (1995). Genetic dissection of complex traits: guidelines for interpreting and reporting linkage results. Nat. Genet. 11:241–247PubMedCrossRefGoogle Scholar
  30. Lankford T. E., Billerbeck J. M., Conover D. O. (2001). Evolution of intrinsic growth and energy acquistion rates ii. Trade-off with vulnerability to predation in Menidia menidia. Evolution 53(9):1873–1881CrossRefGoogle Scholar
  31. Lincoln S., Daly M., Lander E. S. (1992). Mapping genes controlling quantitative traits with MAPMAKER/QTL 1.1. Whitehead Institute Technical Report, Cambridge, MAGoogle Scholar
  32. Lucas M. D., Drew R. E., Wheeler P. A., Verrell P. A., Thorgaard G. H. (2004). Behavioral differences among rainbow trout clonal lines. Behav. Genet. 34:355–365PubMedCrossRefGoogle Scholar
  33. Lynch M., Walsh B. (1998). Genetics and analysis of quantitative traits. Sunderland, MA, Sinauer AssociatesGoogle Scholar
  34. Magurran A. E. (1990). The inheritance and development of minnow antipredator behavior. Anim. Behav. 39:834–842CrossRefGoogle Scholar
  35. Magurran A. E., Seghers B. H., Shaw P. W., Carvalho G. R. (1995). The behavioural diversity and evolution of guppy, Poecilia reticulata, populations in Trinidad. Advances in the Study of Behavior. San Diego, Academic Press Inc, pp. 363–439Google Scholar
  36. Mather K., Jinks J. L. (1982). Biometrical genetics. Cambridge, Chapman and HallGoogle Scholar
  37. Nakamichi R., Ukai Y., Kishino H. (2001). Detection of closely linked multiple quantitative trait loci using a genetic algorithm. Genetics 158:463–475PubMedGoogle Scholar
  38. Orr H. A. (1998). Testing natural selection vs. genetic drift in phenotypic evolution using quantitative trait locus data. Genetics 149(4):2099–2104PubMedGoogle Scholar
  39. Osborne K. A., Robichon A., Burgess E., Butland S., Shaw R. A., Coulthard A., Pereira H. S., Greenspan R. J., Sokolowski M. B. (1997). Natural behavior polymorphism due to a cGMP-dependent protein kinase of Drosophila. Science 277:834–836PubMedCrossRefGoogle Scholar
  40. Pattinson S. (1996). Genetic selection for extensive condition. Appl. Anim. Behav. Sci. 49(1):47–59CrossRefGoogle Scholar
  41. Pavlov D. S., Kasumyan A. O. (2000). Patterns and mechanisms of schooling behavior in fish: A review. J. Ichthyol. 40:163–231Google Scholar
  42. Petersson E., Jarvi T., Steffner N. G., Ragnarsson B. (1996). The effect of domestication on some life history traits of sea trout and atlantic salmon. J. Fish Biol. 48:776–791CrossRefGoogle Scholar
  43. Pitcher T. J. (1992). Who dares wins: The function and evolution of predator inspection behaviour in fish shoals. Neth. J. Zool. 42:371–391CrossRefGoogle Scholar
  44. Pitcher T. J., Parrish J. K. (1993). Functions of shoaling behaviour in teleosts Behaviour Of Teleost Fishes TJ Pitcher. London, Chapman and Hall, pp. 363–439Google Scholar
  45. Planes S., Romans P. (2004). Evidence of genetic selection for growth in new recruits in marine fish. Mol. Ecol. 13(7):2049–2060PubMedCrossRefGoogle Scholar
  46. Price E. O. (1999). Behavioral development in animals undergoing domestication. Applied Anim. Behav. Sci. 65:245–271CrossRefGoogle Scholar
  47. Ranta E., Kaitala V. (1991). School size affects individual feeding success in three-spined sticklebacks (Gasterosteus aculeatus). J. Fish Biol. 39:733–737CrossRefGoogle Scholar
  48. Robison B. D., Wheeler P. A., Sundin K., Sikka P., Thorgaard G. H. (2001). Composite interval mapping reveals a major locus influencing embryonic development rate in rainbow trout (Oncorhyncu mykiss). J. Hered. 92:16–21PubMedCrossRefGoogle Scholar
  49. Robison, B. D., and Rowland. W. (2005). A potential model system for studying the genetics of domestication: behavioral variation among wild and domesticated strains of zebrafish (Danio rerio). Can. J. Fish. Aquat. Sci. 62: 2046–2054CrossRefGoogle Scholar
  50. Ruzzante D. E., Doyle R. W. (1991). Rapid behavioral changes in medaka (Oryzias–Latipes) caused by selection for competitive and noncompetitive growth. Evolution 45:1936–1946CrossRefGoogle Scholar
  51. Ruzzante D. E., Doyle R. W. (1993). Evolution of social-behavior in a resource-rich, structured environment – Selection experiments with medaka (Oryzias–Latipes). Evolution 47:456–470CrossRefGoogle Scholar
  52. Sambrook, J., Fritsch, E. F., and Maniatis, T. (1989). Molecular cloning: A laboratory manual. Cold Spring Harbour Laboratory PressGoogle Scholar
  53. Sawyer L. A., Hennessy J. M., Pexioto A. A., Kyriacou P. (1997). Natural variation in a drosophila clock gene and temperature compensation. Science 278:2117–2120PubMedCrossRefGoogle Scholar
  54. Shin J. T., Fishman M. C. (2002). From zebrafish to human: Molecular medical models. Ann. Rev. Genom. Hum. Genet. 3:311–340CrossRefGoogle Scholar
  55. Tully T. (1996). Discovery of genes involved in learning and memory: An experimental synthesis of Hirschian and Benzerian perspectives. PNAS USA. 93(24):13460–13467PubMedCrossRefGoogle Scholar
  56. Turri M. G., Henderson N. D., DeFries J. C., Flint J. (2001). Quantitative trait locus mapping in laboratory mice derived from a replicated selection experiment for open-field activity. Genetics 158:1217–1226PubMedGoogle Scholar
  57. Wright D., Rimmer L., Pritchard V. L., Krause J., Butlin R. K. (2003). Inter and intra-population variation in shoaling and boldness in the zebrafish (Danio rerio). Naturwiss 90:374–377PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, Inc. 2006

Authors and Affiliations

  • Dominic Wright
    • 1
  • Reiichiro Nakamichi
    • 2
  • Jens Krause
    • 1
  • Roger K. Butlin
    • 3
  1. 1.School of BiologyUniversity of LeedsLeedsUK
  2. 2.Institute of Medical ScienceUniversity of TokyoTokyoJapan
  3. 3.Department of Animal and Plant SciencesThe University of SheffieldSheffieldUK
  4. 4.Department of Animal Breeding and Genetics, BMCUppsala UniversityUppsala Sweden

Personalised recommendations