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Heritability of Boldness and Aggressiveness in the Zebrafish

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Abstract

Behavioural traits that are consistent over time and in different contexts are often referred to as personality traits. These traits influence fitness because they play a major role in foraging, reproduction and survival, and so it is assumed that they have little or no additive genetic variance and, consequently, low heritability because, theoretically, they are under strong selection. Boldness and aggressiveness are two personality traits that have been shown to affect fitness. By crossing single males to multiple females, we estimated the heritability of boldness and aggressiveness in the zebrafish, Danio rerio. The additive genetic variance was statistically significant for both traits and the heritability estimates (95 % confidence intervals) for boldness and aggressiveness were 0.76 (0.49, 0.90) and 0.36 (0.10, 0.72) respectively. Furthermore, there were significant maternal effects accounting for 18 and 9 % of the proportion of phenotypic variance in boldness and aggressiveness respectively. This study shows that there is a significant level of genetic variation in this population that would allow these traits to evolve in response to selection.

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References

  • Ang TZ, Manica A (2010) Benefits and costs of dominance in the angelfish Centropyge bicolour. Ethology 116(9):855–865

    Google Scholar 

  • Ariyomo TO, Watt PJ (2012) The effect of variation in boldness and aggressiveness on the reproductive success of zebrafish, Danio rerio. Anim Behav 83(1):41–46

    Article  Google Scholar 

  • Bell AM, Hankison SJ, Laskowski KL (2009) The repeatability of behaviour: a meta-analysis. Anim Behav 77(4):771–783

    Article  Google Scholar 

  • Bijma P (2011) A general definition of the heritable variation that determines the potential of a population to respond to selection. Genetics 189(4):1347–1359

    Article  PubMed  Google Scholar 

  • Biro PA, Stamps JA (2008) Are animal personality traits linked to life-history productivity? Trends Ecol Evol 23(7):360–368

    Article  Google Scholar 

  • Blomberg SP, Garland TJR, Ives AR (2003) Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution 57(4):717–745

    PubMed  Google Scholar 

  • Boissy A (1995) Fear and fearfulness in animals. Q Rev Biol 70(2):165–191

    Article  PubMed  Google Scholar 

  • Bonduriansky R, Day T (2009) Nongenetic inheritance and its evolutionary implications. Annu Rev Ecol Evol Syst 40:103–125

    Article  Google Scholar 

  • Brown C, Burgess F, Braithwaite VA (2007) Heritable and experiential effects on boldness in a tropical poeciliid. Behav Ecol Sociobiol 62(2):237–243

    Article  Google Scholar 

  • Burns JG (2008) The validity of three tests of temperament in guppies, Poecilia reticulata. J Comp Psychol 122(4):344–356

    Article  PubMed  Google Scholar 

  • Careau V, Thomas D, Pelletier F, Turki L, Landry F, Garant D, Réale D (2011) Genetic correlation between resting metabolic rate and exploratory behaviour in deer mice (Peromyscus maniculatus). J Evol Biol 24(10):2153–2163

    Article  PubMed  Google Scholar 

  • Chervet N, Zöttl M, Schürch R, Taborsky M, Heg D (2011) Repeatability and heritability of behavioural types in a social Cichlid. Int J Evol Biol, Article ID 321729

  • Dahlbom SJ, Lagman D, Lundstedt-Enkel K, Sundström FL, Winberg S (2011) Boldness predicts social status in zebrafish (Danio rerio). PLoS One 6:e23565

    Article  PubMed  Google Scholar 

  • Dahlbom SJ, Backstrom T, Lundstedt-Enkel K et al (2012) Aggression and monoamines: effects of sex and social rank in zebrafish (Danio rerio). Behav Brain Res 228(2):333–338

    Article  PubMed  Google Scholar 

  • Dall SRX, Houston AI, McNamara JM (2004) The behavioural ecology of personality: consistent individual differences from an adaptive perspective. Ecol Lett 7(8):734–739

    Article  Google Scholar 

  • Desjardins JK, Fernald RD (2010) What do fish think of their mirror images? Biol Lett 6(6):744–747

    Article  PubMed  Google Scholar 

  • Dijkstra PD, Schaafsma SM, Hofmann HA, Groothuis TG (2012) ‘Winner effect’ without winning: unresolved social conflicts increase the probability of winning a subsequent contest in a cichlid fish. Physiol Behav 105(2):489–492

    Article  PubMed  Google Scholar 

  • Dingemanse NJ, Realé D (2005) Natural selection and animal personality. Behaviour 142(9–10):1165–1190

    Google Scholar 

  • Dingemanse N, Both C, Drent PJ, Van Oers K, Van Noordwijk AJ (2002) Repeatability and heritability of exploratory behaviour in great tits from the wild. Anim Behav 64(6):929–938

    Article  Google Scholar 

  • Drent PJ, Van Oers K, Van Noordwijk AJ (2003) Realized heritability of personalities in the great tit (Parus major). Proc R Soc Lond B Biol Sci 270(1510):45–51

    Article  Google Scholar 

  • Dyer JR, Croft DP, Morrell LJ, Krause J (2009) Shoal composition determines foraging success in the guppy. Behav Ecol 20(1):165–171

    Article  Google Scholar 

  • Eising CM, Eikenaar C, Groothuis AGG (2001) Maternal androgens in black-headed gull (Larus ridibundus) eggs: consequences for chick development. Proc R Soc Lond B Biol Sci 268(1469):839–846

    Article  Google Scholar 

  • Falconer DS, Mackay TFC (1996) Introduction to quantitative genetics, 4th edn. Longmans Green, Harlow, Essex, UK

    Google Scholar 

  • Filby AL, Paull GC, Hickmore TFA, Tyler CR (2010) Unravelling the neurophysiological basis of aggression in a fish model. BMC Genomics 11:498

    Article  PubMed  Google Scholar 

  • Gerlai R, Lahav M, Guo S, Rosenthal A (2000) Drink like a fish: zebra fish (Danio rerio) as a behaviour genetic model to study alcohol effects. Pharmacol Biochem Behav 67(4):773–782

    Article  PubMed  Google Scholar 

  • Giesing ER, Suski CD, Warner RE, Bell AM (2011) Female sticklebacks transfer information via eggs: effects of maternal experience with predators on offspring. Proc R Soc Lond B Biol Sci 278(1712):1753–1759

    Article  Google Scholar 

  • Gil D (2008) Hormones in avian eggs: physiology, ecology and behavior. Adv Stud Behav 38:337–398

    Article  Google Scholar 

  • Godin J-GJ, Dugatkin LA (1996) Female mating preference for bold males in the guppy, Poecilia reticulata. Proc Natl Acad Sci USA 93(19):10262–10267

    Article  PubMed  Google Scholar 

  • Gosling S (2001) From mice to men: what can we learn about personality from animal research? Psychol Bull 127(1):45–86

    Article  PubMed  Google Scholar 

  • Hadfield J (2010) MCMC Methods for multi-response generalized linear mixed models: The MCMCglmm R Package. http://cran.r-project.org/web/packages/MCMCglmm/vignettes/Overview.pdf

  • Heath DD, Blouw DM (1998) Are maternal effects in fish adaptive or merely physiological side effects? In: Mousseau TA, Fox CW (eds) Maternal effects as adaptation. Oxford University Press, New York, pp 178–201

    Google Scholar 

  • Hirschenhauser K, Wittek M, Johnston P, Mostl E (2008) Social context rather than behavioral output or winning modulates post-conflict testosterone responses in Japanese quail (Coturnix japonica). Physiol Behav 95(3):457–463

    Article  PubMed  Google Scholar 

  • Hoffmann AA (1999) Is the heritability for courtship and mating speed in Drosophila (fruit fly) low? Heredity 82(2):158–162

    Article  PubMed  Google Scholar 

  • Jones JS (1987) The heritability of fitness: bad news for good genes? Trends Ecol Evol 2(2):35–38

    Article  PubMed  Google Scholar 

  • Koolhaas JM, Korte SM, De Boer SF, Van Der Vegt BJ, Van Reenen CG, Hopster H, Hopster H, De Jong IC, Ruis MAW, Blokhuis HJ (1999) Coping styles in animals: current status in behaviour and stress-physiology. Neurosci Biobehav Rev 23(7):925–935

    Article  PubMed  Google Scholar 

  • Kruuk LEB (2004) Estimating genetic parameters in natural populations using the ‘animal model’. Proc R Soc Lond B Biol Sci 359(1446):873–890

    Article  Google Scholar 

  • Kruuk LE, Hadfield JD (2007) How to separate genetic and environmental causes of similarity between relatives. J Evol Biol 20(5):1890–1903

    Article  PubMed  Google Scholar 

  • Larson ET, O’Malley DM, Melloni RH (2006) Aggression and vasotocin are associated with dominante subordinate relationships in zebrafish. Behav Brain Res 167(1):94–102

    Article  PubMed  Google Scholar 

  • Leatherland JF, Li M, Barkataki S (2010) Stressors, glucocorticoids and ovarian function in teleosts. J Fish Biol 76(1):86–111

    Article  PubMed  Google Scholar 

  • Lush JL (1949) Heritability of quantitative characters in farm animals. Hereditas 35(S1):356–375

    Article  Google Scholar 

  • McCormick MI (1998) Behaviorally induced maternal stress in a fish influences progeny quality by a hormonal mechanism. Ecology 79(6):1873–1883

    Article  Google Scholar 

  • McGlothlin JW, Moore AJ, Wolf JB, Brodie ED III (2010) Interacting phenotypes and the evolutionary process. III. Social evolution. Evolution 64(9):2558–2574

    Article  PubMed  Google Scholar 

  • Merilä J, Sheldon BC (1999) Genetic architecture of fitness and nonfitness traits: empirical patterns and development of ideas. Heredity 83(2):103–109

    Article  PubMed  Google Scholar 

  • Moore AJ, Brodie ED III, Wolf JB (1997) Interacting phenotypes and the evolutionary process. I. Direct and indirect genetic effects of social interactions. Evolution 51(5):1352–1362

    Article  Google Scholar 

  • Moretz JA, Martins EP, Robison BD (2007a) Behavioral syndromes and the evolution of correlated behavior in zebrafish. Behav Ecol 18(3):556–562

    Article  Google Scholar 

  • Moretz JA, Martins EP, Robison BD (2007b) The effects of early and adult social environment on zebrafish (Danio rerio) behavior. Environ Biol Fishes 80(1):91–101

    Article  Google Scholar 

  • Mousseau TA, Fox CW (1998) The adaptive significance of maternal effects. Trends Ecol Evol 13(10):403–407

    Article  PubMed  Google Scholar 

  • Norton WH, Stumpenhorst K, Faus-Kessler T, Folchert A, Rohner N, Harris MP, Callebert J, Bally-Cuif L (2011) Modulation of Fgfr1a signaling in zebrafish reveals a genetic basis for the aggression-boldness syndrome. J Neurosci 31(39):13796–13807

    Article  PubMed  Google Scholar 

  • Oliveira RF, Carneiro LA, Canário AVM (2005) No hormonal response in tied fights. Nature 437(7056):207–208

    Article  PubMed  Google Scholar 

  • Olivier B, Young LJ (2002) Animal models of aggression. In: Davis KL, Charney D, Coyle JT, Nemeroff C (eds) Neuropsychopharmacology: the fifth generation of progress. Lippincott Williams and Wilkins, Philadelphia, pp 1699–1708

    Google Scholar 

  • Paull GC, Filby AL, Giddins HG, Coe TS, Hamilton PB, Tyler CR (2010) Dominance hierarchies in zebrafish (Danio rerio) and their relationship with reproductive success. Zebrafish 7(1):109–117

    Article  PubMed  Google Scholar 

  • Qvarnström A, Price TD (2001) Maternal effects, paternal effects and sexual selection. Trends Ecol Evol 16(2):95–100

    Article  PubMed  Google Scholar 

  • R Development Core Team (2011) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.rproject.org

  • Réale D, Festa-Bianchet M (2003) Predator-induced natural selection on temperament in bighorn ewes. Anim Behav 65(3):463–470

    Article  Google Scholar 

  • Réale D, Reader SM, Sol D, McDougall PT, Dingemanse N (2007) Integrating animal temperament within ecology and evolution. Biol Rev 82(2):291–318

    Article  PubMed  Google Scholar 

  • Robison BD, Rowland W (2005) A potential model system for studying the genetics of domestication: behavioral variation among wild and domesticated strains of zebra danio (Danio rerio). Can J Fish Aquat Sci 62(9):2046–2054

    Article  Google Scholar 

  • Schwabl H (1993) Yolk is a source of maternal testosterone for developing birds. Proc Natl Acad Sci USA 90(24):11446–11450

    Article  PubMed  Google Scholar 

  • Sih A, Watters J (2005) The mix matters: behavioural types and group dynamics in water striders. Behaviour 142(9–10):1417–1922

    Article  Google Scholar 

  • Sih A, Bell A, Johnson J (2004a) Behavioral syndromes: an ecological and evolutionary overview. Trends Ecol Evol 19(7):372–378

    Article  PubMed  Google Scholar 

  • Sih A, Bell A, Johnson J, Ziemba R (2004b) Behavioral syndromes: an integrative overview. Q Rev Biol 79(3):241–277

    Article  PubMed  Google Scholar 

  • Sinn D, Apiolaza L, Moltschaniwskyj N (2006) Heritability and fitness-related consequences of squid personality traits. J Evol Biol 19(5):1437–1447

    Article  PubMed  Google Scholar 

  • Smith BR, Blumstein DT (2008) Fitness consequences of personality: a meta-analysis. Behav Ecol 19(2):448–455

    Article  Google Scholar 

  • Smith BR, Blumstein DT (2010) Behavioral types as predictors of survival in trinidadian guppies (Poecilia reticulata). Behav Ecol 21(5):919–926

    Article  Google Scholar 

  • Spence R, Gerlach G, Lawrence C, Smith C (2008) The behaviour and ecology of the zebrefish Danio rerio. Biol Rev 83(1):13–34

    Article  PubMed  Google Scholar 

  • Stamps JA (2007) Growth-mortality tradeoffs and ‘personality traits’ in animals. Ecol Lett 10(5):355–363

    Article  PubMed  Google Scholar 

  • Stamps JA, Groothuis TGG (2010) Developmental perspectives on personality: implications for ecological and evolutionary studies of individual differences. Philos Trans R Soc Lond B Biol Sci 365(1560):4029–4041

    Article  PubMed  Google Scholar 

  • Stirling DG, Réale D, Roff DA (2002) Selection, structure and the heritability of behaviour. J Evol Biol 15(2):277–289

    Article  Google Scholar 

  • Storm JJ, Lima SL (2010) Mothers forewarn offspring about predators: a transgenerational maternal effect on behaviour. Am Nat 175(3):382–390

    Article  PubMed  Google Scholar 

  • Stratholt ML, Donaldson EM, Liley NR (1997) Stress induced elevation of plasma cortisol in adult female coho salmon (Oncorhynchus kisutch), is reflected in egg cortisol content, but does not appear to affect early development. Aquaculture 158(1–2):141–153

    Article  Google Scholar 

  • Taylor RW, Boon AK, Dantzer B, Réale D, Humphries MM, Boutin S, Gorrell JC, Coltman DW, McAdam AG (2012) Low heritabilities, but genetic and maternal correlations between red squirrel behaviours. J Evol Biol 25(4):614–624

    Article  PubMed  Google Scholar 

  • Van Oers K, Drent PJ, de Jong G, van Noordwijk AJ (2004) Additive and nonadditive genetic variation in avian personality traits. Heredity 93(5):496–503

    Article  PubMed  Google Scholar 

  • Waldmann P (2001) Additive and non-additive genetic architecture of two different-sized populations of Scabiosa canescens. Heredity 86(Pt6):648–657

    Article  PubMed  Google Scholar 

  • Watt PJ, Skinner A, Hale M, Nakagawa S, Burke T (2011) Small subordinate male advantage in the zebrafish. Ethology 117(11):1003–1008

    Article  Google Scholar 

  • Wilson DS, Clark AB, Coleman K, Dearstyne T (1994) Shyness and boldness in humans and other animals. Trends Ecol Evol 9(11):442–446

    Article  Google Scholar 

  • Wilson AJ, Gelin U, Perron M-C, Réale D (2009) Indirect genetic effects and the evolution of aggression in a vertebrate system. Proc R Soc Lond B Biol Sci 276(1656):533–541

    Article  Google Scholar 

  • Wilson AJ, Réale D, Clements MN, Morrissey MM, Postma E, Walling CA, Kruuk LEB, Nussey DH (2010) An ecologist’s guide to the animal model. J Anim Ecol 79(1):13–26

    Article  PubMed  Google Scholar 

  • Wisenden BD, Sailer CD, Radenic SJ, Sutrisno R (2011) Maternal inheritance and exploratory-boldness behavioural syndrome in zebrafish. Behaviour 148(14):1443–1456

    Article  Google Scholar 

  • Wolf JB, Brodie ED III, Cheverud JM, Moore AJ, Wade MJ (1998) Evolutionary consequences of indirect genetic effects. Trends Ecol Evol 13(2):64–69

    Article  PubMed  Google Scholar 

  • Wolf JB, Brodie ED III, Moore AJ (1999) Interacting phenotypes and the evolutionary process. II. Selection resulting from social interactions. Am Nat 153(3):254–266

    Article  Google Scholar 

  • Wright D, Rimmer LB, Pritchard VL, Krause J, Butlin RK (2003) Inter and intra-population variation in shoaling and boldness in the zebrafish (Danio rerio). Naturwissenschaften 90(8):374–377

    Article  PubMed  Google Scholar 

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Acknowledgments

We thank Jon Slate for comments on the manuscript, Phil Young for technical assistance and two anonymous reviewers for helpful comments and constructive criticism.

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Authors and Affiliations

  1. Department of Animal and Plant Sciences, University of Sheffield, Western Bank, Sheffield, S10 2TN, UK

    Tolulope O. Ariyomo & Penelope J. Watt

  2. Center for Ecology and Conservation, College of Life and Environmental Sciences, University of Exeter, Cornwall Campus, Penryn, UK

    Mauricio Carter

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  1. Tolulope O. Ariyomo
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  2. Mauricio Carter
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Correspondence to Tolulope O. Ariyomo.

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Ariyomo, T.O., Carter, M. & Watt, P.J. Heritability of Boldness and Aggressiveness in the Zebrafish. Behav Genet 43, 161–167 (2013). https://doi.org/10.1007/s10519-013-9585-y

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