Behavior Genetics

, Volume 45, Issue 2, pp 245–254 | Cite as

Aggressive Behavior, Brain Size and Domestication in Clonal Rainbow Trout Lines

  • Janet M. Campbell
  • Patrick A. Carter
  • Paul A. Wheeler
  • Gary H. ThorgaardEmail author
Original Research


Domestication causes behavior and brain size changes in many species. We addressed three questions using clonal rainbow trout lines: What are the mirror-elicited aggressive tendencies in lines with varying degrees of domestication? How does brain size relate to genotype and domestication level? Finally, is there a relationship between aggressive behavior and brain size? Clonal lines, although sampling a limited subset of the species variation, provide us with a reproducible experimental system with which we can develop hypotheses for further research. We performed principal component analyses on 12 continuous behavior and brain/body size variables and one discrete behavioral variable (“yawn”) and detected several aggression syndromes. Two behaviors, “freeze” and “escape”, associated with high domestication; “display” and “yawn” behavior associated with wild lines and “swim against the mirror” behavior associated with semi-wild and domestic lines. Two brain size traits, total brain and olfactory volume, were significantly related to domestication level when taking total body size into account, with domesticated lines having larger total brain volume and olfactory regions. The aggression syndromes identified indicate that future QTL mapping studies on domestication-related traits would likely be fruitful.


Hatchery Salmonid Aggression Clonal line Mirror test Brain volume 



Funding for this project was provided in part by Agriculture and Food Research Initiative Competitive Grant numbers 2009-35205-05067 and 2011-67015-30091 from the USDA National Institute of Food and Agriculture. We thank Troutlodge Inc., the Washington Department of Fish and Wildlife and the Alaska Department of Fish and Game for providing gametes used in this study. We also thank two anonymous reviewers for their helpful comments.

Conflict of Interest

Janet M. Campbell, Patrick A. Carter, Paul A. Wheeler, and Gary H. Thorgaard declare that they have no conflict of interest.

Human and Animal Rights and Informed Consent

All institutional and national guidelines for the care and use of laboratory animals were followed.


  1. Albert FW, Carlborg O, Plyusnina I, Besnier F, Hedwig D, Lautenschlager S, Lorenz D, McIntosh J, Neumann C, Richter H, Zeising C, Kozhemyakina R, Shchepina O, Kratzsch J, Trut L, Teupser D, Thiery J, Schoneberg T, Andersson L, Paabo S (2009) Genetic architecture of tameness in a rat model of animal domestication. Genetics 182(2):541–554CrossRefPubMedCentralPubMedGoogle Scholar
  2. Araki H, Cooper B, Blouin MS (2007) Genetic effects of captive breeding cause a rapid, cumulative fitness decline in the wild. Science 318(5847):100–103CrossRefPubMedGoogle Scholar
  3. Araki H, Berejikian BA, Ford MJ, Blouin MS (2008) Fitness of hatchery-reared salmonids in the wild. Evol Appl 1(2):342–355CrossRefPubMedCentralPubMedGoogle Scholar
  4. Bellinger KL, Thorgaard GH, Carter PA (2014) Domestication is associated with reduced burst swimming performance and increased body size in clonal rainbow trout lines. Aquaculture 420:154–159Google Scholar
  5. Belyaev D (1978) Destabilizing selection as a factor in domestication. J Hered 70:301–308Google Scholar
  6. Berejikian BA, Mathews SB, Quinn TP (1996) Effects of hatchery and wild ancestry and rearing environments on the development of agonistic behavior in steelhead trout (Oncorhynchus mykiss) fry. Can J Fish Aquat Sci 53(9):2004–2014CrossRefGoogle Scholar
  7. Berejikian BA, Tezak EP, Riley SC, LaRae AL (2001) Competitive ability and social behaviour of juvenile steelhead reared in enriched and conventional hatchery tanks and a stream environment. J Fish Biol 59(6):1600–1613CrossRefGoogle Scholar
  8. Christensen KA, Brunelli JP, Wheeler PA, Thorgaard GH (2014) Antipredator behavior QTL: differences in rainbow trout clonal lines derived from wild and hatchery populations. Behav Genet 44(5):535–546Google Scholar
  9. Conrad JL, Weinersmith KL, Brodin T, Saltz JB, Sih A (2011) Behavioural syndromes in fishes: a review with implications for ecology and fisheries management. J Fish Biol 78(2):395–435CrossRefPubMedGoogle Scholar
  10. Dingemanse NJ, Reale D (2005) Natural selection and animal personality. Behaviour 142:1159–1184Google Scholar
  11. Drew RE, Schwabl H, Wheeler PA, Thorgaard GH (2007) Detection of qtl influencing cortisol levels in rainbow trout (Oncorhynchus mykiss). Aquaculture 272:S183–S194Google Scholar
  12. Ebinger P (1995) Domestication and plasticity of brain organization in mallards (Anas-platyrhynchos). Brain Behav Evol 45(5):286–300CrossRefPubMedGoogle Scholar
  13. Gonda A, Herczeg G, Merila J (2009) Adaptive brain size divergence in nine-spined sticklebacks (Pungitius pungitius)? J Evol Biol 22(8):1721–1726CrossRefPubMedGoogle Scholar
  14. Guay PJ, Iwaniuk AN (2008) Captive breeding reduces brain volume in waterfowl (Anseriformes). Condor 110(2):276–284CrossRefGoogle Scholar
  15. Huntingford FA (2004) Implications of domestication and rearing conditions for the behaviour of cultivated fishes. J Fish Biol 65:122–142Google Scholar
  16. Iguchi K, Matsubara N, Hakoyama H (2001) Behavioural individuality assessed from two strains of cloned fish. Anim Behav 61:351–356Google Scholar
  17. Jensen P (2014) Behavior genetics and the domestication of animals. Annu Rev Anim Biosci 2(1):85–104CrossRefPubMedGoogle Scholar
  18. Kihslinger RL, Nevitt GA (2006) Early rearing environment impacts cerebellar growth in juvenile salmon. J Exp Biol 209(3):504–509CrossRefPubMedGoogle Scholar
  19. Kihslinger RL, Lema SC, Nevitt GA (2006) Environmental rearing conditions produce forebrain differences in wild chinook salmon Oncorhynchus tshawytscha. Comp Biochem Physiol A 145(2):145–151CrossRefGoogle Scholar
  20. Kolm N, Gonzalez-Voyer A, Brelin D, Winberg S (2009) Evidence for small scale variation in the vertebrate brain: mating strategy and sex affect brain size and structure in wild brown trout (Salmo trutta). J Evol Biol 22(12):2524–2531CrossRefPubMedGoogle Scholar
  21. Korzan WJ, Summers CH (2007) Behavioral diversity and neurochemical plasticity: selection of stress coping strategies that define social status. Brain Behav Evol 70(4):257–266CrossRefPubMedGoogle Scholar
  22. Kukekova AV, Trut LN, Chase K, Kharlamova AV, Johnson JL, Temnykh SV, Oskina IN, Gulevich RG, Vladimirova AV, Klebanov S, Shepeleva DV, Shikhevich SG, Acland GM, Lark KG (2011) Mapping loci for fox domestication: deconstruction/reconstruction of a behavioral phenotype. Behav Genet 41(4):593–606CrossRefPubMedCentralPubMedGoogle Scholar
  23. Lichatowich J (2013) Salmon, people and place: a biologist’s search for salmon recovery. Oregon State University Press, CorvallisGoogle Scholar
  24. Lucas MD, Drew RE, Wheeler PA, Verrell PA, Thorgaard GH (2004) Behavioral differences among rainbow trout clonal lines. Behav Genet 34(3):355–365CrossRefPubMedGoogle Scholar
  25. Marchetti MP, Nevitt GA (2003) Effects of hatchery rearing on brain structures of rainbow trout, Oncorhynchus mykiss. Environ Biol Fish 66(1):9–14CrossRefGoogle Scholar
  26. McDougall PT, Reale D, Sol D, Reader SM (2006) Wildlife conservation and animal temperament: causes and consequences of evolutionary change for captive, reintroduced, and wild populations. Anim Conserv 9(1):39–48CrossRefGoogle Scholar
  27. Mery F, Burns JG (2010) Behavioural plasticity: an interaction between evolution and experience. Evol Ecol 24(3):571–583CrossRefGoogle Scholar
  28. Millot S, Péan S, Labbé L, Kerneis T, Quillet E, Dupont-Nivet M, Bégout M-L (2014) Assessment of genetic variability of fish personality traits using rainbow trout isogenic lines. Behav Genet 44(4):383–393Google Scholar
  29. Nichols KM, Broman KW, Sundin K, Young JM, Wheeler PA, Thorgaard GH (2007) Quantitative trait loci x maternal cytoplasmic environment interaction for development rate in Oncorhynchus myhiss. Genetics 175(1):335–347CrossRefPubMedCentralPubMedGoogle Scholar
  30. Nichols KM, Edo AF, Wheeler PA, Thorgaard GH (2008) The genetic basis of smoltification-related traits in Oncorhynchus mykissi. Genetics 179(3):1559–1575CrossRefPubMedCentralPubMedGoogle Scholar
  31. O’Regan HJ, Kitchener AC (2005) The effects of captivity on the morphology of captive, domesticated and feral mammals. Mamm Rev 35(3–4):215–230CrossRefGoogle Scholar
  32. Pollen AA, Dobberfuhl AP, Scace J, Igulu MM, Renn SCP, Shumway CA, Hofmann HA (2007) Environmental complexity and social organization sculpt the brain in lake tanganyikan cichlid fish. Brain Behav Evol 70(1):21–39CrossRefPubMedGoogle Scholar
  33. Reale D, Reader SM, Sol D, McDougall PT, Dingemanse NJ (2007) Integrating animal temperament within ecology and evolution. Biol Rev 82(2):291–318CrossRefPubMedGoogle Scholar
  34. Rehkamper G, Frahm HD, Cnotka J (2008) Mosaic evolution and adaptive brain component alteration under domestication seen on the background of evolutionary theory. Brain Behav Evol 71(2):115–126CrossRefPubMedGoogle Scholar
  35. Reinbold D, Thorgaard GH, Carter PA (2009) Reduced swimming performance and increased growth in domesticated rainbow trout, oncorhynchus mykiss. Can J Fish Aquat Sci 66(7):1025–1032CrossRefGoogle Scholar
  36. Robison BD, Thorgaard GH (2004) The phenotypic relationship of a clonal line to its population of origin: rapid embryonic development in an alaskan population of rainbow trout. Trans Am Fish Soc 133(2):455–461CrossRefGoogle Scholar
  37. Robison BD, Wheeler PA, Thorgaard GH (1999) Variation in development rate among clonal lines of rainbow trout (Oncorhynchus mykiss). Aquaculture 173(1–4):131–141CrossRefGoogle Scholar
  38. Schjolden J, Winberg S (2007) Genetically determined variation in stress responsiveness in rainbow trout: behavior and neurobiology. Brain Behav Evol 70(4):227–238CrossRefPubMedGoogle Scholar
  39. Schjolden J, Backstrom T, Pulman KGT, Pottinger TG, Winberg S (2005a) Divergence in behavioural responses to stress in two strains of rainbow trout (Oncorhynchus mykiss) with contrasting stress responsiveness. Horm Behav 48(5):537–544CrossRefPubMedGoogle Scholar
  40. Schjolden J, Stoskhus A, Winberg S (2005b) Does individual variation in stress responses and agonistic behavior reflect divergent stress coping strategies in juvenile rainbow trout? Physiol Biochem Zool 78(5):715–723CrossRefPubMedGoogle Scholar
  41. Schutz KE, Kerje S, Jacobsson L, Forkman B, Carlborg O, Andersson L, Jensen P (2004) Major growth qtls in fowl are related to fearful behavior: possible genetic links between fear responses and production traits in a red junglefowl × white leghorn intercross. Behav Genet 34(1):121–130CrossRefPubMedGoogle Scholar
  42. Sih A, Bell AM, Johnson JC, Ziemba RE (2004) Behavioral syndromes: an integrative overview. Q Rev Biol 79(3):241–277CrossRefPubMedGoogle Scholar
  43. Sinn DL, Moltschaniwskyj NA (2005) Personality traits in dumpling squid (Euprymna tasmanica): context-specific traits and their correlation with biological characteristics. J Comp Psychol 119(1):99–110CrossRefPubMedGoogle Scholar
  44. Sinn DL, Gosling SD, Moltschaniwskyj NA (2008) Development of shy/bold behaviour in squid: context-specific phenotypes associated with developmental plasticity. Anim Behav 75:433–442Google Scholar
  45. Sloman KA, Wilson RW, Balshine S (2006) Behaviour and physiology of fish. Elsevier, AmsterdamGoogle Scholar
  46. Sundin K, Brown KH, Drew RE, Nichols KM, Wheeler PA, Thorgaard GH (2005) Genetic analysis of a development rate qtl in backcrosses of clonal rainbow trout, Oncorhynchus mykiss. Aquaculture 247(1–4):75–83CrossRefGoogle Scholar
  47. Swallow JG, Carter PA, Garland T (1998) Artificial selection for increased wheel-running behavior in house mice. Behav Genet 28(3):227–237Google Scholar
  48. Takahashi A, Tomihara K, Shiroishi T, Koide T (2010) Genetic mapping of social interaction behavior in b6/msm consomic mouse strains. Behav Genet 40(3):366–376CrossRefPubMedCentralPubMedGoogle Scholar
  49. Tuomainen U, Candolin U (2011) Behavioural responses to human-induced environmental change. Biol Rev 86(3):640–657CrossRefPubMedGoogle Scholar
  50. Ward DM, Nislow KH, Armstrong JD, Einum S, Folt CL (2007) Is the shape of the density-growth relationship for stream salmonids evidence for exploitative rather than interference competition? J Anim Ecol 76(1):135–138CrossRefPubMedGoogle Scholar
  51. Williams JG, Zabel RW, Waples RS, Hutchings JA, Connor WP (2008) Potential for anthropogenic disturbances to influence evolutionary change in the life history of a threatened salmonid. Evol Appl 1(2):271–285CrossRefPubMedCentralPubMedGoogle Scholar
  52. Wright D, Nakamichi R, Krause J, Butlin RK (2006) Qtl analysis of behavioral and morphological differentiation between wild and laboratory zebrafish (Danio rerio). Behav Genet 36(2):271–284CrossRefPubMedGoogle Scholar
  53. Young WP, Wheeler PA, Fields RD, Thorgaard GH (1996) DNA fingerprinting confirms isogenicity of androgenetically derived rainbow trout lines. J Hered 87(1):77–81CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  • Janet M. Campbell
    • 1
    • 2
  • Patrick A. Carter
    • 1
  • Paul A. Wheeler
    • 1
  • Gary H. Thorgaard
    • 1
    Email author
  1. 1.School of Biological Sciences and Center for Reproductive BiologyWashington State UniversityPullmanUSA
  2. 2.Thermo Fisher ScientificIntrinsic BioProbes MSIA TechnologiesTempeUSA

Personalised recommendations