Unravelling the proximate causes of the aggression-boldness behavioural syndrome in zebrafish

Behaviour

Volumn 149, Issue 10-12, 2012, Pages 1063-1079

  Norton, W H J ^a   Bally Cuif, L ^a  

^a CNRS   (France)

Author keywords

aggression; behaviour; behavioural syndrome; boldness; exploration; proximate cause; zebrafish

Indexed keywords

ANIMALIA; DANIO RERIO;

EID: 84870353679     PISSN: 00057959     EISSN: 1568539X     Source Type: Journal    
DOI: 10.1163/1568539X-00003012     Document Type: Review

References (86)

1. Arnqvist, G. & Henriksson, S. (1997). Sexual cannibalism in the fishing spider and a model for the evolution of sexual cannibalism based on genetic constraints. - Evol. Ecol. 11: 255-273.
2. Basquill, S.P. & Grant, J.W.A. (1997). An increase in habitat complexity reduces aggression and monopolization of food by zebrafish (Danio rerio). - Can. J. Zool. 76: 770-772.
3. Bell, A.M. (2005). Behavioural differences between individuals and two populations of stickleback (Gasterosteus aculeatus). - J. Evol. Biol. 18: 464-473. (Pubitemid 40350941)
4. Bell, A.M. & Sih, A. (2007). Exposure to predation generates personality in threespined sticklebacks (Gasterosteus aculeatus). - Ecol. Lett. 10: 828-834. (Pubitemid 47174413)
5. Bencan, Z., Sledge, D. & Levin, E.D. (2009). Buspirone, chlordiazepoxide and diazepam effects in a zebrafish model of anxiety. - Pharmacol. Biochem. Behav. 94: 75-80.
6. Benus, R.F., Bohus, B., Koolhaas, J.M. & van Oortmerssen, G.A. (1991). Heritable variation for aggression as a reflection of individual coping strategies. - Experientia 47: 1008- 1019.
7. Biro, P.A. & Stamps, J.A. (2008). Are animal personality traits linked to life-history productivity? - Trends Ecol. Evol. 23: 361-368. (Pubitemid 351847646)
8. Blaser, R.E. & Rosemberg, D.B. (2012). Measures of anxiety in zebrafish (Danio rerio): dissociation of black/white preference and novel tank test. - PLoS One 7: e36931.
9. Block, J. (1995). A contrarian view of the five-factor approach to personality description. - Psychol. Bull. 117: 187-215.
10. Boissy, A. (1995). Fear and fearfulness in animals. - Q. Rev. Biol. 70: 165-191.
11. Bourne, G.R. & Sammons, A.J. (2008). Boldness, aggression and exploration: evidence for a behavioural syndrome in male pentamorphic livebearing fish, Poecilia parae. - AACL Bioflux 1: 39-49.
12. Braida, D., Donzelli, A.,Martucci, R., Capurro, V., Busnelli, M., Chini, B. & Sala,M. (2012). Neurohypophyseal hormones manipulation modulate social and anxiety-related behavior in zebrafish. - Psychopharmacology (Berlin) 220: 319-330.
13. Brick, O. & Jakobsson, S. (2001). Individual variation in risk taking: the effect of a predatory threat on fighting behavior in Nannacara anomola. - Behav. Ecol. 13: 439-442. (Pubitemid 34793667)
14. Brown, C., Gardner, C. & Braithwaite, V.A. (2005). Differential stress responses in fish from areas of high- and low-predation pressure. - J. Comp. Physiol. B 175: 305-312. (Pubitemid 40938469)
15. Budaev, S. & Andrew, R.J. (2009). Patterns of early embryonic light exposure determine behavioural asymmetries in zebrafish: a habenular hypothesis. - Behav. Brain Res. 200: 91-94.
16. Cachat, J., Canavello, P., Elegante, M., Bartels, B., Hart, P., Bergner, C., Egan, R., Duncan, A., Tien, D., Chung, A., Wong, K., Goodspeed, J., Grimes, C., Elkhayat, S., Suciu, C., Rosenberg, M., Chung, K., Kadri, F., Roy, S., Gaikwad, S., Stewart, A., Zapolsky, I., Gilder, T., Mohnot, S., Beeson, E., Tan, J., Amri, H., Zukowska, A., Glasgow, E., Soignier, R. & Kalueff, A. (2010a). Modeling withdrawal syndrome in zebrafish. - Behav. Brain Res. 208: 371-376.
17. Cachat, J., Stewart, A., Grossman, L., Gaikwad, S., Kadri, F., Chung, K.M., Wu, N., Wong, K., Roy, S., Suciu, C., Goodspeed, J., Elegante, M., Bartels, B., Elkhayat, S., Tien, D., Tan, J., Denmark, A., Gilder, T., Kyzar, E., Dileo, J., Frank, K., Chang, K., Utterback, E., Hart, P. & Kalueff, A.V. (2010b). Measuring behavioral and endocrine responses to novelty stress in adult zebrafish. - Nature Protocols 5: 1786-1799.
18. Colman, J.R., Baldwin, D., Johnson, L.L. & Scholz, N.L. (2009). Effects of the synthetic estrogen, 17α-ethinylestradiol, on aggression and courtship behavior in male zebrafish (Danio rerio). - Aquat. Toxicol. 91(4): 346-354
19. Conrad, J.L., Weinersmith, K.L., Brodin, T., Saltz, J.B. & Sih, A. (2011). Behavioural syndromes in fishes: a review with implications for ecology and fisheries management. - J. Fish. Biol. 78: 395-435.
20. Dadda, M., Domenichini, A., Piffer, L., Argenton, F. & Bisazza, A. (2010). Early differences in epithalamic left-right asymmetry influence lateralization and personality of adult zebrafish. - Behav. Brain Res. 206: 208-215.
21. Dahlbom, S.J., Lagman, D., Lundstedt-Enkel, K., Sundstrom, L.F. & Winberg, S. (2011). Boldness predicts social status in zebrafish (Danio rerio). - PLoS One 6(8): e23565.
22. Dahlbom, S.J., Backstrom, T., Lundstedt-Enkel, K. & Winberg, S. (2012). Aggression and monoamines: effects of sex and social rank in zebrafish (Danio rerio). - Behav. Brain Res. 228: 333-338.
23. Dahm, R. & Geisler, R. (2006). Learning from small fry: the zebrafish as a genetic model organism for aquaculture fish species. - Mar. Biotechnol. 8: 329-345. (Pubitemid 44221541)
24. Dall, S.R.X., Houston, A.I. & McNamara, J.M. (2004). The behavioural ecology of personality: consistent individual differences from an adaptive prospective. - Ecol. Lett. 7: 734-739. (Pubitemid 39040218)
25. Deng, C.X., Wynshaw-Boris, A., Shen, M.M., Daugherty, C., Ornitz, D.M. & Leder, P. (1994). Murine FGFR-1 is required for early postimplantation growth and axial organization. - Genes Dev. 8: 3045-3057.
26. Desjardins, J.K. & Fernald, R.D. (2010). What do fish make of mirror images? - Biol. Lett. 6: 744-747.
27. Dingemanse, N.J. & Wolf, M. (2010). Recent models for adaptive personality differences: a review. - Philos. Trans. Roy. Soc. Lond. B: Biol. 365: 3947-3958.
28. Dingemanse, N.J.,Wright, J., Kazem, A.J., Thomas, D.K., Hickling, R.&Dawnay, N. (2007). Behavioural syndromes differ predictably between 12 populations of three-spined stickleback. - J. Anim. Ecol. 76: 1128-1138. (Pubitemid 47547430)
29. Dingemanse, N.J., Kazem, A.J., Reale, D. & Wright, J. (2010). Behavioural reaction norms: animal personality meets individual plasticity. - Trends Ecol. Evol. 25: 81-89.
30. Dugatkin, L.A. & Druen, M. (2004). The social implications of winner and loser effects. - Proc. Biol. Sci. 271(Suppl. 6): S488-S489.
31. Dzieweczynski, T.L. & Leopard, A.K. (2010). The effects of stimulus type on consistency of responses to conflicting stimuli in Siamese fighting fish. - Behav. Proc. 85: 83-89.
32. Egan, R.J., Bergner, C.L., Hart, P.C., Cachat, J.M., Canavello, P.R., Elegante, M.F., Elkhayat, S.I., Bartels, B.K., Tien, A.K., Tien, D.H., Mohnot, S., Beeson, E., Glasgow, E., Amri, H., Zukowska, Z. & Kalueff, A.V. (2009). Understanding behavioral and physiological phenotypes of stress and anxiety in zebrafish. - Behav. Brain Res. 205: 38-44.
33. Filby, A.L., Paull, G.C., Hickmore, T.F. & Tyler, C.R. (2010). Unravelling the neurophysiological basis of aggression in a fish model. - BMC Genomics 11: 498.
34. Filby, A.L., Paull, G.C., Searle, F., Ortiz-Zarragoitia, M. & Tyler, C.R. (2012). Environmental estrogen-induced alterations of male aggression and dominance hierarchies in fish: a mechanistic analysis. - Environ. Sci. Technol. 46: 3472-3479.
35. Flint, J., Corley, R., 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: 1432-1435.
36. Force, A., Lynch, M., Pickett, F.B., Amores, A., Yan, Y.L. & Postlethwait, J. (1999). Preservation of duplicate genes by complementary, degenerative mutations. - Genetics 151: 1531-1545. (Pubitemid 29177561)
37. Fraser, D.F., Gilliam, J.F., Daley, M.J., Le, A.N. & Skalski, G.T. (2001). Explaining leptokurtic movement distributions: intrapopulation variation in boldness and exploration. - Am. Nat. 158: 124-135. (Pubitemid 32682539)
38. Frost, A.J., Winrow-Giffen, A., Ashley, P.J. & Sneddon, L.U. (2007). Plasticity in animal personality traits: does prior experience alter the degree of boldness?. - Proc. Biol. Sci. 274: 333-339. (Pubitemid 47055456)
39. Gerlai, R., Lahav, M., Guo, S. & Rosenthal, A. (2000). Drinks like a fish: zebra fish (Danio rerio) as a behavior genetic model to study alcohol effects. - Pharmacol. Biochem. Behav. 67: 773-782. (Pubitemid 32144928)
40. Grosenick, L., Clement, T.S. & Fernald, R.D. (2007). Fish can infer social rank by observation alone. - Nature 445: 429-432. (Pubitemid 46160910)
41. Huang, P., Xiao, A., Zhou, M., Zhu, Z., Lin, S. & Zhang, B. (2011). Heritable gene targeting in zebrafish using customized TALENs. - Nature Biotechnol. 29: 699-700.
42. Huntingford, F.A. (1976). The relationship between anti-predator behaviour and aggression among conspecifics in the three-spined stickleback, Gasterosteus aculeatus. - Anim. Behav. 24: 245-260.
43. Ketterson, E.D. & Nolan, V. (1992). Hormones and life histories: an integrative approach. - Am. Nat. 140(Suppl. 1): S33-S62. (Pubitemid 23398811)
44. Koolhaas, J.M., Korte, S.M., de Boer, S.F., van der Vegt, B.J., van Reenen, C.G., Hopster, H., De Jong, I.C., Ruis, M.A. & Blokhuis, H.J. (1999). Coping styles in animals: current status in behavior and stress-physiology. - Neurosci. Biobehav. Rev. 23: 925-935. (Pubitemid 29502398)
45. Larson, E.T., OMalley, D.M. & Melloni Jr., R.H. (2006). Aggression and vasotocin are associated with dominant-subordinate relationships in zebrafish. - Behav. Brain Res. 167: 94-102. (Pubitemid 43063143)
46. Lecklin, A., Etu-Seppala, P., Stark, H. & Tuomisto, L. (1998). Effects of intracerebroventricularly infused histamine and selective H1, H2 and H3 agonists on food and water intake and urine flow in Wistar rats. - Brain Res. 793: 279-288. (Pubitemid 28294095)
47. Lorenz, K. (1966). On aggression. - Routledge, London. Lynn, S.E., Egar, J.M.,Walker, B.G., Sperry, T.S. & Ramenofsky, M. (2007). Fish on Prozac: a simple, noninvasive physiology laboratory investigating the mechanisms of aggressive behavior in Betta splendens. - Adv. Physiol. Educ. 31: 358-363.
48. Marks, C., West, T.N., Bagatto, B. & Moore, F.B.-G. (2005). Developmental environment alters conditional aggression in zebrafish. - Copeia: 901-908. (Pubitemid 43058150)
49. Martin, J.G. & Reale, D. (2008). Animal temperament and human disturbance: implications for the response of wildlife to tourism. - Behav. Proc. 77: 66-72. (Pubitemid 350235821)
50. Masaki, T. & Yoshimatsu, H. (2006). The hypothalamic H1 receptor: a novel therapeutic target for disrupting diurnal feeding rhythm and obesity. - Trends Pharmacol. Sci. 27: 279-284.
51. Maupin, J.L. & Riechert, S.E. (2001). Superfluous killing in spiders: a consequence of adaptation to food-limited environments? - Behav. Ecol. 12: 569-576. (Pubitemid 32882186)
52. Maximino, C., da Silva, A.W., Gouveia Jr., A. & Herculano, A.M. (2011). Pharmacological analysis of zebrafish (Danio rerio). scototaxis. - Prog. Neuropsychopharmacol. Biol. Psychol. 35: 624-631.
53. Moore, A.J., Brodie, E.D. & Wolf, J.B. (1997). Interacting phenotypes and the evolutionary process. 1.
54. Direct and indirect genetic effects of social interactions. - Evolution 51: 1352- 1362.
55. Moretz, J.A., Martins, E.P.&Robison, B.D. (2007). Behavioural syndromes and the evolution of correlated behavior in zebrafish. - Behav. Ecol. 18: 556-562. (Pubitemid 47355615)
56. Norton, W.H., Stumpenhorst, K., Faus-Kessler, T., Folchert, A., Rohner, N., Harris, M.P., Callebert, J. & Bally-Cuif, L. (2011). Modulation of Fgfr1a signaling in zebrafish reveals a genetic basis for the aggression-boldness syndrome. - J. Neurosci. 31: 13796-13807.
57. Oliveira, R.F., Carneiro, L.A. & Canario, A.V. (2005). Behavioural endocrinology: no hormonal response in tied fights. - Nature 437: 207-208. (Pubitemid 41294476)
58. Parker, M.O., Millington, M.E., Combe, F.J. & Brennan, C.H. (2012). Development and implementation of a three-choice serial reaction time task for zebrafish (Danio rerio). - Behav. Brain Res. 227: 73-80.
59. Passani, M.B., Lin, J.S., Hancock, A., Crochet, S. & Blandina, P. (2004). The histamine H3 receptor as a novel therapeutic target for cognitive and sleep disorders. - Trends Pharmacol. Sci. 25: 618-625. (Pubitemid 39458167)
60. Paull, G.C., Filby, A.L., Giddins, H.G., Coe, T.S., Hamilton, P.B. & Tyler, C.R. (2010). Dominance hierarchies in zebrafish (Danio rerio) and their relationship with reproductive success. - Zebrafish 7: 109-117.
61. Peake, T.M. &McGregor, P.K. (2004). Information and aggression in fishes. - Learn. Behav. 32: 114-121. (Pubitemid 38585884)
62. Peitsaro, N., Kaslin, J., Anichtchik, O.V.& Panula, P. (2003).Modulation of the histaminergic system and behaviour by α-fluoromethylhistidine in zebrafish. - J. Neurochem. 86: 432- 441.
63. Reale, D., Reader, S.M., Sol, D., McDougall, P.T. & Dingemanse, N.J. (2007). Integrating animal temperament within ecology and evolution. - Biol. Rev. Camb. Phil. Soc. 82: 291-318. (Pubitemid 46587935)
64. Rosemberg, D.B., Braga, M.M., Rico, E.P., Loss, C.M., Cordova, S.D., Mussulini, B.H., Blaser, R.E., Leite, C.E., Campos,M.M., Dias, R.D., Calcagnotto, M.E., de Oliveira, D.L. & Souza, D.O. (2012). Behavioral effects of taurine pretreatment in zebrafish acutely exposed to ethanol. - Neuropharmacology 63: 613-623.
65. Sander, J.D., Cade, L., Khayter, C., Reyon, D., Peterson, R.T., Joung, J.K. & Yeh, J.R. (2011). Targeted gene disruption in somatic zebrafish cells using engineered TALENs. - Nature Biotechnol. 29: 697-698.
66. Schjolden, J., Backstrom, T., Pulman, K.G., Pottinger, T.G. &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. (Pubitemid 41662291)
67. Sih, A. & Bell, A.M. (2007). Insights from behavioural syndromes for the evolutionary genetics of personality. - Eur. J. Personal. 21: 626-628.
68. Sih, A., Bell, A. & Johnson, J.C. (2004). Behavioral syndromes: an ecological and evolutionary overview. - Trends Ecol. Evol. 19: 372-378. (Pubitemid 38800923)
69. Sledge, D., Yen, J., Morton, T., Dishaw, L., Petro, A., Donerly, S., Linney, E. & Levin, E.D. (2011). Critical duration of exposure for developmental chlorpyrifos-induced neurobehavioral toxicity. - Neurotoxicol. Teratol. 33: 742-751.
70. Sneddon, L.U., Schmidt, R., Fang, Y. & Cossins, A.R. (2011). Molecular correlates of social dominance: a novel role for ependymin in aggression. - PLoS One 6: e18181.
71. Stewart, A., Cachat, J., Wong, K., Gaikwad, S., Gilder, T., DiLeo, J., Chang, K., Utterback, E. & Kalueff, A.V. (2010). Homebase behavior of zebrafish in novelty-based paradigms. - Behav. Proc. 85: 198-203.
72. Thisse, B. &Thisse, C. (2005). Functions and regulations of fibroblast growth factor signaling during embryonic development. - Dev. Biol. 287: 390-402. (Pubitemid 41636772)
73. Tropepe, V. & Sive, H.L. (2003). Can zebrafish be used as a model to study the neurodevelopmental causes of autism?. - Genes Brain Behav. 2: 268-281. (Pubitemid 37345665)
74. Veenema, A.H., Meijer, O.C., de Kloet, E.R. & Koolhaas, J.M. (2003). Genetic selection for coping style predicts stressor susceptibility. - J. Neuroendocrinol. 15: 256-267. (Pubitemid 36266893)
75. Wada, H., Inagaki, N., Yamatodani, A. & Watanabe, T. (1991). Is the histaminergic neuron system a regulatory center for whole-brain activity. - Trends Neurosci. 14: 415-418.
76. Williams, L.R., Wong, K., Stewart, A., Suciu, C., Gaikwad, S., Wu, N., Dileo, J., Grossman, L., Cachat, J., Hart, P. & Kalueff, A.V. (2012). Behavioral and physiological effects of RDX on adult zebrafish. - Comp. Biochem. Physiol. C: Toxicol. Pharmacol. 155: 33- 38.
77. Wilson, A.D.M. & Godin, J.G.J. (2009). Boldness and behavioral syndromes in the bluegill sunfish, Lepomis macrochirus. - Behav. Ecol. 20: 231-237.
78. Wilson, D.S. (1998). Adaptation and natural selection for the masses. - Trends Ecol. Evol. 13: 39-40.
79. Wilson, D.S., Clark, A.B., Coleman, K. & Dearstyne, T. (1994). Shyness and boldness in humans and other animals. - Trends Ecol. Evol. 9: 442-446. (Pubitemid 124001495)
80. Wolf, M. & Weissing, F.J. (2010). An explanatory framework for adaptive personality differences. - Philos. Trans. R. Soc. Lond. B: Biol. 365: 3959-3968.
81. Wolf, M., van Doorn, G.S., Leimar, O. &Weissing, F.J. (2007). Life-history trade-offs favour the evolution of animal personalities. - Nature 447: 581-584. (Pubitemid 46868040)
82. Wright, D., Nakamichi, R., Krause, J. & Butlin, R.K. (2006). QTL analysis of behavioral and morphological differentiation between wild and laboratory zebrafish (Danio rerio). - Behav. Genet. 36: 271-284. (Pubitemid 43673569)
83. Wright, D., Rimmer, L.B., Pritchard, V.L., Krause, J. & Butlin, R.K. (2003). Inter and intrapopulation variation in shoaling and boldness in the zebrafish (Danio rerio). - Naturwissenschaften 90: 374-377. (Pubitemid 37129960)
84. Wyart, C. & Del Bene, F. (2011). Let there be light: zebrafish neurobiology and the optogenetic revolution. - Rev. Neurosci. 22: 121-130.
85. Yamaguchi, A., Ishii, H., Morita, I., Oota, I. & Takeda, H. (2004). mRNA expression of fibroblast growth factors and hepatocyte growth factor in rat plantaris muscle following denervation and compensatory overload. - Pflugers Arch. 448: 539-546. (Pubitemid 39141532)
86. Yanai, K., Son, L.Z., Endou, M., Sakurai, E., Nakagawasai, O., Tadano, T., Kisara, K., Inoue, I., Watanabe, T. & Watanabe, T. (1998). Behavioural characterization and amounts of brain monoamines and their metabolites in mice lacking histamine H1 receptors. - Neuroscience 87: 479-487. (Pubitemid 28370904)