Assessment of Genetic Variability of Fish Personality Traits using Rainbow Trout Isogenic Lines

Abstract

The study of inter-individual variability of personality in fish is a growing field of interest but the genetic basis of this complex trait is still poorly investigated due to the difficulty in controlling fish genetic origin and life history. When available, isogenic lines that allow performing independent tests on different individuals having identical genotype constitute a very relevant experimental material to disentangle the genetic and environmental components of behavioural individuality. We took advantage of heterozygous isogenic lines to investigate the personality in rainbow trout through the analysis of their reactions to different experimental situations. To this end, seven to ten rainbow trout isogenic lines were screened for their spatial exploratory behaviour, their flight response toward a stressor and their risk taking behaviour. Results showed that some lines seemed less sensitive to new events or environmental changes and could be defined as low responsive, while others were very sensitive and defined as high responsive. The use of isogenic lines highlighted the importance of genetic factors, in combination with life history, in the expression of personality in domesticated fish.

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References

  1. Aragon P, Meylan S, Clobert J (2006) Dispersal status—dependent response to the social environment in the Common Lizard, Lacerta vivipara. Funct Ecol 20:900–907

    Article  Google Scholar 

  2. Bell AM (2005) Behavioural differences between individuals and two populations of stickleback (Gasterosteus aculeatus). J Evol Biol 18:464–473

    PubMed  Article  Google Scholar 

  3. Bell A, Stamps JA (2004) Development of behavioural differences between individuals and populations of sticklebacks, Gasterosteus aculeatus. Anim Behav 68:1339–1348

    Article  Google Scholar 

  4. Berejikian BA (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 52:2476–2482

    Article  Google Scholar 

  5. Boissy A, Bouissou MF (1995) Assessment of individual differences in behavioural reactions of heifers exposed to various fear-eliciting situations. Appl. Anim. Behav. Sci. 46:17–31

    Article  Google Scholar 

  6. Boujard T, Labbe L, Auperin B (2002) Feeding behaviour, energy expenditure and growth of rainbow trout in relation to stocking density and food accessibility. Aquac Res 33:1233–1242

    Article  Google Scholar 

  7. Brown GE, Smith RJF (1997) Conspecific skin extracts elicit antipredator responses in juvenile rainbow trout (Oncorhynchus mykiss). Can J Zool 75:1916–1922

    Article  Google Scholar 

  8. Cote J, Fogarty S, Weinersmith K, Brodin T, Sih A (2010) Personality traits and dispersal tendency in the invasive mosquitofish (Gambusia affinis). Proc R Soc B: Biol Sci 277:1571–1579

    Article  Google Scholar 

  9. Dagnélie P (1975) Théorie et méthodes statistiques, applications agronomiques, vol 2. Presses Agronomiques de Gembloux, Gembloux

    Google Scholar 

  10. Dingemanse NJ, Kazem AJN, Réale D, Wright J (2010) Behavioural reaction norms: animal personality meets individual plasticity. Trends Ecol Evol 25:81–89

    PubMed  Article  Google Scholar 

  11. Drangsholt TMK, Damsgård B, Olesen I (2014) Quantitative genetics of behavioral responsiveness in Atlantic cod (Gadus morhua L.). Aquaculture 420–421:282–287

    Article  Google Scholar 

  12. Drew RE, Schwabl H, Wheeler PA, Thorgaard GH (2007) of QTL influencing cortisol levels in rainbow trout (Oncorhynchus mykiss). Aquaculture 272S1:S183–S194

    Article  Google Scholar 

  13. Feldker DEM, Datson NA, Veenema AH, Meulmeester E, De Kloet ER, Vreugdenhil E (2003) Serial analysis of gene expression predicts structural differences in hippocampus of long attack latency and short attack latency mice. Eur J Neurosci 17:379–387

    PubMed  Article  Google Scholar 

  14. Fevolden SE, Røed KH (1993) Cortisol and immune characteristics in rainbow trout (Onchorhynchus mykiss) selected for high or low tolerance to stress. J Fish Biol 43:919–930

    Article  Google Scholar 

  15. Fevolden SE, Refstie T, Røed KH (1991) Selection for high and low cortisol stress response in Atlantic salmon (Salmo salar) and rainbow trout (Oncorhynchus mykiss) selected for stress response. Aquaculture 104:19–29

    Article  Google Scholar 

  16. Fevolden SE, Røed KH, Gjedrem B (1993) Genetic components of post-stress cortisol and lysozyme activity in Atlantic salmon; correlations to disease resistance. Fish Shellfish Immunol 4:507–519

    Article  Google Scholar 

  17. Giles N, Huntingford FA (1984) Predation risk and interpopulation variation in anti-predator behaviour in the three-spined stickleback, Gasterosteus aculeatus L. Anim Behav 32:264–275

    Article  Google Scholar 

  18. Iguchi K, Matsubara N, Hakoyama H (2001) Behavioural individuality assessed from two strains of cloned fish. Anim Behav 61:351–356

    Article  Google Scholar 

  19. Johnsson JI, Abrahams MV (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 48:243–247

    Article  Google Scholar 

  20. Johnsson JI, Petersson E, Jönsson E, Björnsson BT, Järvi T (1996) Domestication and growth hormone alter antipredator behaviour and growth patterns in juvenile brown trout, Salmo trutta. Can J Fish Aquat Sci 53:1546–1554

    Article  Google Scholar 

  21. Koolhaas JM, Korte SM, De Boer SF, Van Der Vegt BJ, Van Reenen CG, Hopster H, De Jong IC, Ruis MAW, Blokhuis HJ (1999) Coping styles in animals: current in behavior and stress-physiology. Neurosci Biobehav Rev 23:925–935

    PubMed  Article  Google Scholar 

  22. Krause J, Hoare D, Krause S, Hemelrijk CK, Rubenstein D (2000) Leadership in fish shoals. Fish Fish 1:82–89

    Article  Google Scholar 

  23. Le Neindre P, Boivin X, Boissy A (1996) Handling of extensively kept animals. Appl Anim Behav Sci 49:73–81

    Article  Google Scholar 

  24. Leblond C, Reebs SG (2006) Individual leadership and boldness in shoals of golden shiners (Notemigonus crysoleucas). Behaviour 143:1263–1280

    Article  Google Scholar 

  25. Lucas M, Drew R, Wheeler P, Verrell P, Thorgaard G (2004) Behavioral differences among rainbow trout clonal lines. Behav Genet 34:355–365

    PubMed  Article  Google Scholar 

  26. Martin EP (1991) Individual and sex differences in the use of the push-up display by the sagebush lizard, Sceloporus graciosus. Anim Behav 41:403–416

    Article  Google Scholar 

  27. Millot S, Bégout ML, Person-Le Ruyet J, Breuil G, Di-Poï C, Fievet J, Pineau P, Roué M, Sévère A (2008) Feed demand behavior in sea bass juveniles: effects on individual specific growth rate variation and health (inter-individual and inter-group variation). Aquaculture 274:87–95

    Article  Google Scholar 

  28. Millot S, Bégout ML, Chatain B (2009a) Exploration behaviour and flight response toward a stimulus in three sea bass strains (Dicentrarchus labrax L.). Appl Anim Behav Sci 119:108–114

    Article  Google Scholar 

  29. Millot S, Bégout ML, Chatain B (2009b) Risk-taking behaviour variation over time in sea bass Dicentrarchus labrax: effects of day-night alterations, fish phenotypic characteristics and selection for growth. J Fish Biol 75:1733–1749

    PubMed  Article  Google Scholar 

  30. Øverli Ø, Winberg S, Pottinger TG (2005) Behavioral and neuroendocrine correlates of selection for stress responsiveness in rainbow trout—a review. Integr Comp Biol 45:463–474

    PubMed  Article  Google Scholar 

  31. Øverli Ø, Sørensen C, Nilsson GE (2006a) Behavioral indicators of stress-coping style in rainbow trout: do males and females react differently to novelty? Physiol Behav 87:506–512

    PubMed  Article  Google Scholar 

  32. Øverli Ø, Sorensen C, Kiessling A, Pottinger TG, Gjoen HM (2006b) Selection for improved stress tolerance in rainbow trout (Onchorhynchus mykiss) leads to reduced feed waste. Aquaculture 261:776–781

    Article  Google Scholar 

  33. Øverli Ø, Sorensen C, Pulman KGT, Pottinger TG, Korzan W, Summers CH, Nilsson GE (2007) Evolutionary background for stress-coping styles: relationships between physiological, behavioral, and cognitive traits in non-mammalian vertebrates. Neurosci Biobehav Rev 31:396–412

    PubMed  Article  Google Scholar 

  34. Pickering AD (1992) Rainbow trout husbandry-management of the stress response. Aquaculture 100:125–139

    Article  Google Scholar 

  35. Pickering AD (1993) Growth and stress in fish production. Aquaculture 111:51–63

    Article  Google Scholar 

  36. Pottinger TG (2006) Context dependent differences in growth of two rainbow trout (Oncorhynchus mykiss) lines selected for divergent stress responsiveness. Aquaculture 256:140–147

    Article  Google Scholar 

  37. Pottinger TG, Carrick TR (1999) Modification of the plasma cortisol response to stress in rainbow trout by selective breeding. Gen Comp Endocrinol 116:122–132

    PubMed  Article  Google Scholar 

  38. Price EO (1998) Behavioral genetics and the process of animal domestication. In: Grandin T (ed) Genetics and the behavior of domestic animals. Academic Press, San Diego, pp 41–65

    Google Scholar 

  39. Price EO (1999) Behavioral development in animals undergoing domestication. Appl Anim Behav Sci 65:245–271

    Article  Google Scholar 

  40. Quillet E, Krieg F, Dechamp N, Hervet C, Bérard A, Le Roy P, Guyomard R, Prunet P, Pottinger TG (2014) QTL for magnitude of the plasma cortisol response to confinement in rainbow trout. Anim Genet 45(2):223–234

    PubMed  Article  Google Scholar 

  41. Quillet E, Dorson M, Le Guillou S, Benmansour A, Boudinot P (2007) Wide range of susceptibility to rhabdovirues in homozygous clones of rainbow trout. Fish Shellfish Immunol 22:510–519

    PubMed  Article  Google Scholar 

  42. Réale D, Reader SM, Sol D, McDougall PT, Dingemanse NJ (2007) Integrating animal temperament within ecology and evolution. Biol Rev 82:291–318

    PubMed  Article  Google Scholar 

  43. Rexroad C, Vallejo R, Liu S, Palti Y, Weber G (2012) QTL affecting stress response to crowding in a rainbow trout broodstock population. BMC Genet 13:97

    PubMed Central  PubMed  Article  Google Scholar 

  44. Rexroad C, Vallejo R, Liu S, Palti Y, Weber G (2013) Quantitative trait loci affecting response to crowding stress in an F2 generation of rainbow trout produced through phenotypic selection. Mar Biotechnol 15:613–627

    PubMed  Article  Google Scholar 

  45. Riechert SE, Hedrick AV (1993) A test for correlations among fitness-linked behavioural traits in the spider Agelenopsis aperta. Anim Behav 46:669–675

    Article  Google Scholar 

  46. Schjolden J, Backström T, Pulman KGT, Pottinger TG, Winberg S (2005) Divergence in behavioural responses to stress in two strains of rainbow trout (Oncorhynchus mykiss) with contrasting stress responsiveness. Horm Behav 48:537–544

    PubMed  Article  Google Scholar 

  47. Sih A, Bell A, Johnson JC (2004) Behavioral syndromes: an ecological and evolutionary overview. Trends Ecol Evol 19:372–378

    PubMed  Article  Google Scholar 

  48. Slater PJB (1981) Individual differences in animal behaviour. In: Perspectives in Ethology Vol. 4 (Ed. By D.L.G. Noakes, D.G. Linquist, G.S. Helfman and J.A. Ward). The Hague: W. Junk. pp.159-171

  49. Sokal RR, Rohlf FJ (1995) Biometry. The principles and practice of statistics in biological research. New York, NY: W.H. Freeman and Company

  50. Van Oers K, de Jong G, van Noordwijk AJ, Kempenaers B, Drent PJ (2005) Contribution of genetics to the study of animal personalities: a review of case studies. Behaviour 142:1185–1206

    Article  Google Scholar 

  51. Vrijenhoek RC (1994) Unisexual fish: model systems for studying ecology and evolution. Ann Rev Ecol Syst 24:71–96

    Article  Google Scholar 

  52. Weber GM, Silverstein JT (2007) Evaluation of a stress response for use in a selective breeding program for improved growth and disease resistance in Rainbow trout. N Am J Aquacult 69:69–79

    Article  Google Scholar 

  53. Weber GM, Vallejo RL, Lankford SE, Silverstein JT, Welch TJ (2008) Cortisol response to a crowding stress: heritability and association with disease resistance to Yersinia ruckeri in rainbow trout. N Am J Aquacult 70:425–433

    Article  Google Scholar 

  54. Wisenden BD, Chivers DP, Brown GE, Smith RJF (1995) The role of experience in risk assessment: avoidance of areas chemically labeled with fathead minnow alarm pheromone by conspecifics and heterospecifics. Ecoscience 2:116–122

    Google Scholar 

  55. Wolf M, van Doorn GS, Weissing FJ (2008) Evolutionary emergence of responsive and unresponsive personalities. PNAS 105:15825–15830

    PubMed Central  PubMed  Article  Google Scholar 

  56. Wright D, Butlin R, Carlborg Ö (2006) Epistatic regulation of behavioural and morphological traits in the zebrafish (Danio rerio). Behav Genet 36:914–922

    PubMed  Article  Google Scholar 

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Acknowledgments

This research project has been supported by ANR ADD COSADD No 06-PADD-05. The authors are grateful to Didier Leguay and Michel Prineau for their technical assistance.

Conflict of Interest

The authors declare that they have no conflict of interest.

Human and Animal Rights and Informed Consent

All procedures followed were in accordance with the ethical standards of the responsible committee on human experimentation (institutional and national) and with the Helsinki Declaration of 1975, as revised in 2000 (5). Informed consent was obtained from all patients for being included in the study.

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Correspondence to Sandie Millot.

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Edited by Stephen Maxson.

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Millot, S., Péan, S., Labbé, L. et al. Assessment of Genetic Variability of Fish Personality Traits using Rainbow Trout Isogenic Lines. Behav Genet 44, 383–393 (2014). https://doi.org/10.1007/s10519-014-9652-z

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Keywords

  • Personality
  • Isogenic lines
  • Genetic variability
  • Risk taking
  • Spatial exploration
  • Oncorhynchus mykiss