Behavioral Ecology and Sociobiology

, Volume 70, Issue 1, pp 179–187 | Cite as

On plasticity of aggression: influence of past and present predation risk, social environment and sex

  • Gábor HerczegEmail author
  • Nurul Izza Ab Ghani
  • Juha Merilä
Original Article


Behaviours are phenotypically very plastic traits, allowing fast changes and fine-tuning of trait expression in response to situational demands. Aggression is a behaviour for which the right decisions can have immediate fitness consequences. Hence, the right behavioural decision is expected to be influenced by both past experience and the current environment. Using a factorial common garden experiment, we tested how past and presently perceived predation risk, as well as the social environment during development, and sex affected two components of intraspecific aggression (viz. hesitation to attack and attack intensity) in a social fish species, the three-spined stickleback (Gasterosteus aculeatus). Exposure to predator cues during development affected how fish responded to actual predation risk: exposed fish hesitated more, while predator-naive fish attacked more in the presence of predators. Sociality also had a strong effect: fish grown in pairs hesitated less than fish grown in solitude or in shoals, whereas solitary-grown fish attacked more than conspecific-experienced (i.e. pair or shoal reared) fish. Female aggression was even across the different developmental environments and lower than that of males. Predator- and conspecific-naive males were more aggressive than other males, suggesting that males have high innate aggression levels that are mediated by environmental risk. The results demonstrate complex underpinnings to plasticity-driven behavioural variation and draw attention to the fact that interpretations of presence/absence of an expected behavioural response may be difficult if it is influenced by both past and present environmental conditions.


Behavioural plasticity Development Gasterosteus Predation Sociality Stickleback 



We thank Marika Hölttä and Mirva Turtiainen for their help in obtaining the broodstock as well for help during the fish rearing. Kirsi Kähkönen and Sami Karja kindly helped with the lab work, and Jacquelin DeFaveri provided comments that improved an earlier version of this manuscript. We are also indebted to three anonymous reviewers for their constructive comments. The experiment was supported by the Academy of Finland (grants 129662, 134728 and 218343 to JM; grant 128716 to GH) and the University of Putra Malaysia (to INAG). GH was supported by the Hungarian Scientific Research Fund (grant OTKA-K 105517) and the János Bólyai Research Scholarship of the Hungarian Academy of Sciences during analyses and writing. The experiments were conducted under the licence (no. STH211A) from the Finnish National Animal Experiment Board.

Compliance with ethical standards

All applicable international, national and/or institutional guidelines for the care and use of animals were followed. All procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted. The experiments were conducted under the licence (no. STH211A) from the Finnish National Animal Experiment Board.

Supplementary material

265_2015_2037_MOESM1_ESM.xlsx (23 kb)
ESM 1 (XLSX 23 kb)


  1. Auld JR, Agrawal AA, Relyea RA (2010) Re-evaluating the costs and limits of adaptive phenotypic plasticity. Proc R Soc Lond B 277:503–511CrossRefGoogle Scholar
  2. Bakker TCM (1985) Two-way selection for aggression in juvenile, female and male sticklebacks (Gasterosteus aculeatus L.), with some note on hormonal factors. Behaviour 93:69–81CrossRefGoogle Scholar
  3. Bakker TCM (1986) Aggressiveness of sticklebacks (Gasterosteus aculeatus L.): a behaviour-genetic study. Behaviour 98:1–144CrossRefGoogle Scholar
  4. Bakker TCM (1994a) Evolution of aggressive behaviour in the threespine stickleback. In: Bell MA, Foster SA (eds) The evolutionary biology of threespine stickleback. Oxford University Press, Oxford, UK, pp 345–380Google Scholar
  5. Bakker TCM (1994b) Genetic correlations and the control of behavior, exemplified by aggressiveness in sticklebacks. Adv Stud Behav 23:135–171CrossRefGoogle Scholar
  6. Bell AM (2005) Behavioural differences between individuals and two populations of stickleback (Gasterosteus aculeatus). J Evol Biol 18:464–473PubMedCrossRefGoogle Scholar
  7. Bell MA, Foster SA (1994) The evolutionary biology of threespine stickleback. Oxford University Press, OxfordGoogle Scholar
  8. Bell AM, Sih A (2007) Exposure to predation generates personality in threespined sticklebacks (Gasterosteus aculeatus). Ecol Lett 10:828–834PubMedCrossRefGoogle Scholar
  9. Bell AM, Hankison SJ, Laskowski KL (2009) The repeatability of 908 behaviour: a meta-analysis. Anim Behav 77:771–783Google Scholar
  10. Biro PA, Post JR, Parkinson EA (2003) Density-dependent mortality is mediated by foraging activity for prey fish in whole-lake experiments. J Anim Ecol 72:546–555CrossRefGoogle Scholar
  11. Biro PA, Abrahams MV, Post JR, Parkinson EA (2006) Behavioural trade-offs between growth and mortality explain evolution of submaximal growth rates. J Anim Ecol 75:1165–1171PubMedCrossRefGoogle Scholar
  12. Breden F, Scott MA, Michel E (1987) Genetic differentiation for anti-predator behaviour in the Trinidad guppy, Poecilia reticulata. Anim Behav 35:618–620CrossRefGoogle Scholar
  13. Brown GE, Brown JA, Srivastava RK (1992) The effect of stocking density on the behaviour of Arctic charr Salvellinus alpinus L.). J Fish Biol 41:955–963CrossRefGoogle Scholar
  14. Crispo E (2007) The Baldwin effect and genetic assimilation: revisiting two mechanisms of evolutionary change mediated by phenotypic plasticity. Evolution 61:2469–2479PubMedCrossRefGoogle Scholar
  15. Cubaynes S, MacNulty DR, Stahler DR, Quimby KA, Smith DW, Coulson T (2014) Density-dependent intraspecific aggression regulates survival in northern Yellowstone wolves (Canis lupus). J Anim Ecol 83:1344–1356PubMedCrossRefGoogle Scholar
  16. de Jong G (2005) Evolution of phenotypic plasticity: patterns of plasticity and the emergence of ecotypes. New Phytol 166:101–117PubMedCrossRefGoogle Scholar
  17. DeWitt T, Sih A, Wilson DS (1998) Costs and limits of phenotypic plasticity. Trends Ecol Evol 13:77–81PubMedCrossRefGoogle Scholar
  18. Dingemanse NJ, Wright J, Kazem AJN, Thomas DK, Hickling R, Dawnay N (2007) Behavioural syndromes differ predictably between 12 populations of three-spined stickleback. J Anim Ecol 76:1128–1138PubMedCrossRefGoogle Scholar
  19. Dingemanse NJ, Kazem AJN, Reale D, Wright J (2010) Behavioural reaction norms: animal personality meets individual plasticity. Trends Ecol Evol 25:81–89PubMedCrossRefGoogle Scholar
  20. DiRienzo N, Pruitt JN, Hedrick AV (2012) Juvenile exposure to acoustic signals from conspecifics alters growth trajectory and an adult personality trait. Anim Behav 84:861–868CrossRefGoogle Scholar
  21. Elgar MA (1988) Predator vigilance and group size in mammals and birds: a critical review of the empirical evidence. Biol Rev 64:13–33CrossRefGoogle Scholar
  22. Falconer DS (1952) The problem of environment and selection. Am Nat 86:293–298CrossRefGoogle Scholar
  23. Gabriel W (1999) Evolution of reversible plastic responses: inducible defenses and environmental tolerance. In: Tollrian R, Harwell CD (eds) The ecology and evolution of inducible defenses. Princeton University Press, Princeton, pp 286–305Google Scholar
  24. Garamszegi LZ, Herczeg G (2012) Behavioural syndromes, syndrome deviation and the within- and between-individual components of phenotypic correlations: when reality does not meet statistics. Behav Ecol Sociobiol 66:1651–1658CrossRefGoogle Scholar
  25. Gibson G (2005) The synthesis and evolution of a supermodel. Science 307:1890–1891PubMedCrossRefGoogle Scholar
  26. Gonda A, Herczeg G, Merilä J (2009) Habitat-dependent and -independent plastic responses to social environment in the nine-spined stickleback (Pungitius pungitius) brain. Proc R Soc Lond B 276:2085–2092CrossRefGoogle Scholar
  27. Heins DC (2012) A research programme in fish ecology leads to a supermodel: a tribute to Professor Robert J. Wootton. Ecol Freshw Fish 21:323–324CrossRefGoogle Scholar
  28. Herczeg G, Välimäki K (2011) Intraspecific variation in behaviour: effects of evolutionary history, ontogenetic experience and sex. J Evol Biol 24:2434–2444PubMedCrossRefGoogle Scholar
  29. Herczeg G, Gonda A, Merilä J (2009a) Predation mediated population divergence in complex behaviour of nine-spined stickleback (Pungitius pungitius). J Evol Biol 22:544–552PubMedCrossRefGoogle Scholar
  30. Herczeg G, Gonda A, Merilä J (2009b) The social cost of shoaling covaries with predation risk in nine-spined stickleback (Pungitius pungitius) populations. Anim Behav 77:575–580CrossRefGoogle Scholar
  31. Huntingford FA, Ruiz-Gomez ML (2009) Three-spined sticklebacks Gasterosteus aculeatus as a model for exploring behavioural biology. J Fish Biol 75:1943–1976PubMedCrossRefGoogle Scholar
  32. Jandt JM, Bengston S, Pinter-Wollman N, Pruitt JN, Raine NE, Dornhaus A, Sih A (2014) Behavioural syndromes and social insects: personality at multiple levels. Biol Rev 89:48–67PubMedCrossRefGoogle Scholar
  33. Kaspersson R, Höjesjö J, Pedersen S (2010) Effects of density on foraging success and aggression in age-structured groups of brown trout. Anim Behav 79:709–715CrossRefGoogle Scholar
  34. Kawecki TJ, Ebert D (2004) Conceptual issues in local adaptation. Ecol Lett 7:1225–1241CrossRefGoogle Scholar
  35. Krause J, Ruxton GD (2002) Living in Groups. Oxford University Press, OxfordGoogle Scholar
  36. Laurila A (2000) Behavioural responses to predator chemical cues and local variation in antipredator performance in Rana temporaria tadpoles. Oikos 88:159–168CrossRefGoogle Scholar
  37. Lima SL, Dill LM (1990) Behavioural decisions made under the risk of predation: a review and prospectus. Can J Zool 68:619–640CrossRefGoogle Scholar
  38. Magurran AE, Seghers BH (1991) Variation in schooling and aggression amongst guppy (Poecilia reticulata) populations in Trinidad. Behaviour 118:214–234CrossRefGoogle Scholar
  39. Magurran AE, Seghers BH (1994) Predator inspection behaviour covaries with schooling tendency amongst wild guppy, Poecilia reticulata. Behaviour 128:121–134CrossRefGoogle Scholar
  40. Murtaugh PA (2009) Performance of several variable-selection methods applied to real ecological data. Ecol Lett 12:1061–1068PubMedCrossRefGoogle Scholar
  41. Nakagawa S, Schielzeth H (2010) Repeatability for Gaussian and non-Gaussian data: a practical guide for biologists. Biol Rev 85:935–956PubMedGoogle Scholar
  42. Nakagawa S, Schielzeth H (2013) A general and simple method for obtaining R2 from generalized linear mixed-effect models. Methods Ecol Evol 4:133–142CrossRefGoogle Scholar
  43. Orizaola G, Dahl E, Laurila A (2012) Reversibility of predator-induced plasticity and its effect at a life-history switch point. Oikos 121:44–52CrossRefGoogle Scholar
  44. Peichel K, Ross JA, Matson CK, Dickson M, Grimwood J, Schmutz J, Myers RM, Mori S, Schluter D, Kingsley DM (2004) The master sex determination locus in threespine sticklebacks in a nascent Y chromosome. Curr Biol 14:1416–1424PubMedCrossRefGoogle Scholar
  45. Pfennig DW, Wund MA, Snell-Rood EC, Cruickshank T, Schlichting CD, Moczek AP (2010) Phenotypic plasticity’s impacts on diversification and speciation. Trends Ecol Evol 25:459–467PubMedCrossRefGoogle Scholar
  46. Pigliucci M, Murren CJ, Schlichting CD (2006) Phenotypic plasticity and evolution by genetic assimilation. J Exp Biol 209:2362–2367PubMedCrossRefGoogle Scholar
  47. Pitcher TJ, Parrish JK (1993) Functions of shoaling behaviour in teleosts. In: Pitcher TJ (ed) Behaviour of teleost fishes, 2nd. Chapman & Hall, London, pp 363–439CrossRefGoogle Scholar
  48. Relyea RA (2001) Morphological and behavioral plasticity of larval anurans in response to different predators. Ecology 82:523–540CrossRefGoogle Scholar
  49. Riechert SE, Hedrick AV (1990) Levels of predation and genetically based antipredator behaviour in the spider, Agelenopsis aperta. Anim Behav 40:679–687CrossRefGoogle Scholar
  50. Roff DA (1992) The Evolution of Life Histories. Chapman & Hall, New YorkGoogle Scholar
  51. Selya AS, Rose JS, Dierker LC, Hedeker D, Mermelstein RJ (2012) A practical guide to calculate Cohen’s f2, a measure of local effect size, from PROC MIXED. Front Psychol 3:111PubMedPubMedCentralCrossRefGoogle Scholar
  52. Simmons LW (1986) Inter-male competition and mating success in the field cricket, Gryllus bimaculatus (De Geer). Anim Behav 34:567–579CrossRefGoogle Scholar
  53. Stearns SC (1992) The Evolution of Life Histories. Oxford University Press, New YorkGoogle Scholar
  54. Tinbergen N (1951) The study of instinct. Oxford University Press, New YorkGoogle Scholar
  55. Tollrian R, Harvell CD (1999) The ecology and evolution of inducible defenses. Princeton University Press, PrincetonGoogle Scholar
  56. Van Buskirk J, Arioli M (2005) Habitat specialization and adaptive phenotypic divergence of anuran populations. J Evol Biol 18:596–608PubMedCrossRefGoogle Scholar
  57. Van Buskirk J, Steiner UK (2009) The fitness costs of developmental canalization and plasticity. J Evol Biol 22:852–860PubMedCrossRefGoogle Scholar
  58. West-Eberhard MJ (2003) Developmental plasticity and evolution. Oxford University Press, OxfordGoogle Scholar
  59. Wootton RJ (1970) Aggression in the early phases of the reproductive cycle of the male three-spined stickleback. Anim Behav 18:740–746CrossRefGoogle Scholar
  60. Yoon J, Sillett TS, Morrison SA, Ghalambor CK (2012) Breeding density, not life history, predicts interpopulation differences in territorial aggression in a passerine bird. Anim Behav 84:515–521CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Gábor Herczeg
    • 1
    • 2
    Email author
  • Nurul Izza Ab Ghani
    • 2
    • 3
  • Juha Merilä
    • 2
  1. 1.Behavioural Ecology Group, Department of Systematic Zoology and EcologyEötvös Loránd UniversityBudapestHungary
  2. 2.Ecological Genetics Research Unit, Department of BiosciencesUniversity of HelsinkiHelsinkiFinland
  3. 3.Department of Biology, Faculty of ScienceUniversity of Putra MalaysiaDarul EhsanMalaysia

Personalised recommendations