Behavioral Ecology and Sociobiology

, Volume 70, Issue 6, pp 975–980 | Cite as

Unsociable juvenile male three-spined sticklebacks grow more attractive

  • Sin-Yeon Kim
  • Alberto Velando
Original Article


An animal’s personality may be an adaptive behavioral response of individuals to consistent differences in physiology and life-history. Studying the relationship between behavior and other fitness-related traits within the pace-of-life syndrome (POLS) framework, which explains the integration of different traits using the concept of a fast-slow life-history continuum, may thus be a useful approach to understanding the evolution and maintenance of animal personality. According to the POLS hypothesis, for example, fast individuals should be behaviorally more active, bolder or less sociable, and potentially invest more in reproduction than slow individuals. Here, we examined whether the sociability of juvenile sticklebacks (Gasterosteus aculeatus) is linked with their key reproductive traits, carotenoid-based nuptial coloration of males and egg production of females. We also tested whether experimental manipulation of environmental conditions (control vs. warm winter) can change pace-of-life and the link between behavioral and reproductive traits. Male sticklebacks prone to shoaling expressed lower peak red coloration at the reproductive stage, during which they were solitary and territorial. In females, fecundity was not correlated with early social behavior. Experimental sticklebacks reared in warm winter conditions decreased their investment in reproduction, but the negative relationship between sociability and sexual signal of males was maintained. Our results suggest that the POLS could partly explain the maintenance of personality under predation pressure or severe mating competition. In natural environments, any benefit to sociable male sticklebacks may be counterbalanced by the cost of growing less attractive.

Significance statement

Why do animals vary in personality, and how is such variation maintained within a population? An interesting approach for understanding this is studying how personality traits are correlated with other fitness-related traits within the pace-of-life framework. For the first time, our results show the link between sociability at the juvenile stage and the expression of sexual ornament during reproduction in male three-spined sticklebacks. Sociable juveniles may benefit from reduced predation risk, but they grow less attractive and this may reduce their mating success during reproduction. Thus, the trade-off between survival and reproduction may contribute to the maintenance of among-individual variation in behavior.


Animal personality Carotenoid Fecundity Pace-of-life Sexual signal Shoaling 



We thank three anonymous reviewers for constructive comments and J. Dominguez, A. Gonzalez, and J. Díaz for help during the study.

Compliance with ethical standards

Wild fish were sampled under permission from the Xunta de Galicia (021/2013), and the experiment was approved by the Animal Ethics Committee of the University of Vigo (17/2012 and 10/2014).


Funding was provided by the Spanish Ministerio de Economía y Competitividad (CGL2012-40229-C02-02 and CGL2014-60291-JIN) and the Xunta de Galicia (2012/305).

Conflict of interest

The authors declare that they have no competing interests.


  1. Alonso-Alvarez C, Pérez-Rodríguez L, Garcia JT, Viñuela J (2009) Testosterone-mediated trade-offs in the old age: a new approach to the immunocompetence handicap and carotenoid-based sexual signalling. Proc R Soc Lond B 276:2093–2101CrossRefGoogle Scholar
  2. Bakker TCM (1994) Evolution of aggressive behaviour in the threespine stickleback. In: Bell MA, Foster SA (eds) The evolutionary biology of the threespine stickleback. Oxford University Press, Oxford, pp 345–380Google Scholar
  3. Bell AM, Sih A (2007) Exposure to predation generates personality in threespined sticklebacks (Gasterosteus aculeatus). Ecol Lett 10:828–834CrossRefPubMedGoogle Scholar
  4. Biro PA, Stamps JA (2008) Are animal personality traits linked to life-history productivity? Trends Ecol Evol 23:361–368CrossRefPubMedGoogle Scholar
  5. Biro PA, Stamps JA (2010) Do consistent individual differences in metabolic rate promote consistent individual differences in behavior? Trends Ecol Evol 25:653–659CrossRefPubMedGoogle Scholar
  6. Black C, Scott R, Bernards M (2014) Seasonal changes in carotenoid and lipid storage by threespine stickleback, Gasterosteus aculeatus. Environ Biol Fish 97:209–214CrossRefGoogle Scholar
  7. Bridger D, Bonner SJ, Briffa M (2015) Individual quality and personality: bolder males are less fecund in the hermit crab Pagurus bernhardus. Proc R Soc B 282:20142492CrossRefPubMedPubMedCentralGoogle Scholar
  8. Brown C, Braithwaite VA (2004) Size matters: a test of boldness in eight populations of the poeciliid Brachyraphis episcopi. Anim Behav 68:1325–1329CrossRefGoogle Scholar
  9. Candolin U (1999) Male–male competition facilitates female choice in sticklebacks. Proc R Soc Lond B 266:785–789CrossRefGoogle Scholar
  10. Candolin U (2000) Changes in expression and honesty of sexual signalling over the reproductive lifetime of sticklebacks. Proc R Soc Lond B 267:2425–2430CrossRefGoogle Scholar
  11. Careau V, Thomas D, Humphries M, Réale D (2008) Energy metabolism and animal personality. Oikos 117:641–653CrossRefGoogle Scholar
  12. Careau V, Bininda‐Emonds O, Thomas D, Réale D, Humphries M (2009) Exploration strategies map along fast–slow metabolic and life-history continua in muroid rodents. Funct Ecol 23:150–156CrossRefGoogle Scholar
  13. Dingemanse NJ, Wolf M (2010) Recent models for adaptive personality differences: a review. Philos T Roy Soc B 365:3947–3958CrossRefGoogle Scholar
  14. Dingemanse NJ, van der Plas F, Wright J, Réale D, Schrama M, Roff DA, van der Zee E, Barber I (2009) Individual experience and evolutionary history of predation affect expression of heritable variation in fish personality and morphology. Proc R Soc Lond B 276:1285–1293CrossRefGoogle Scholar
  15. Gosling SD (2001) From mice to men: what can we learn about personality from animal research? Psychol Bull 127:45–86CrossRefPubMedGoogle Scholar
  16. Hofmann HA, Beery AK, Blumstein DT, Couzin ID, Earley RL, Hayes LD, Hurd PL, Lacey EA, Phelps SM, Solomon NG (2014) An evolutionary framework for studying mechanisms of social behavior. Trends Ecol Evol 29:581–589CrossRefPubMedGoogle Scholar
  17. Kim S-Y (2016) Fixed behavioural plasticity in response to predation risk in the three-spined stickleback. Anim Behav 112:147–152CrossRefGoogle Scholar
  18. Kim S-Y, Velando A (2014) Stickleback males increase red coloration and courtship behaviours in the presence of a competitive rival. Ethology 120:502–510CrossRefGoogle Scholar
  19. Kim S-Y, Velando A (2015) Phenotypic integration between antipredator behavior and camouflage pattern in juvenile sticklebacks. Evolution 69:830–838CrossRefPubMedGoogle Scholar
  20. Kim S-Y, Metcalfe NB, Velando A (2016) A benign juvenile environment reduces the strength of antagonistic pleiotropy and genetic variation in the rate of senescence. J Anim Ecol. doi: 10.1111/1365-2656.12468 PubMedGoogle Scholar
  21. Krause J, Ruxton GD (2002) Living in groups. Oxford University Press, OxfordGoogle Scholar
  22. Lackey A, Boughman J (2013) Divergent sexual selection via male competition: ecology is key. J Evol Biol 26:1611–1624CrossRefPubMedGoogle Scholar
  23. Le Galliard J-F, Paquet M, Cisel M, Montes‐Poloni L (2013) Personality and the pace‐of‐life syndrome: variation and selection on exploration, metabolism and locomotor performances. Funct Ecol 27:136–144CrossRefGoogle Scholar
  24. Lee W-S, Monaghan P, Metcalfe NB (2012) The pattern of early growth trajectories affects adult breeding performance. Ecology 93:902–912CrossRefPubMedGoogle Scholar
  25. Lee W-S, Monaghan P, Metcalfe NB (2013) Experimental demonstration of the growth rate–lifespan trade-off. Proc R Soc B 280:20122370CrossRefPubMedPubMedCentralGoogle Scholar
  26. Lewandowski E, Boughman J (2008) Effects of genetics and light environment on colour expression in threespine sticklebacks. Biol J Linn Soc 94:663–673CrossRefGoogle Scholar
  27. Luttbeg B, Sih A (2010) Risk, resources and state-dependent adaptive behavioural syndromes. Philos Tran R Soc B 365:3977–3990CrossRefGoogle Scholar
  28. Magurran A, Maciás Garcia C (2000) Sex differences in behaviour as an indirect consequence of mating system. J Fish Biol 57:839–857CrossRefGoogle Scholar
  29. McGraw KJ, Correa SM, Adkins-Regan E (2006) Testosterone upregulates lipoprotein status to control sexual attractiveness in a colorful songbird. Behav Ecol Sociobiol 60:117–122CrossRefGoogle Scholar
  30. Nicolaus M, Tinbergen JM, Bouwman KM, Michler SP, Ubels R, Both C, Kempenaers B, Dingemanse NJ (2012) Experimental evidence for adaptive personalities in a wild passerine bird. Proc R Soc Lond B 279:4885–4892CrossRefGoogle Scholar
  31. O’Connell LA, Hofmann HA (2011) Genes, hormones, and circuits: an integrative approach to study the evolution of social behavior. Front Neuroendocrinol 32:320–335CrossRefPubMedGoogle Scholar
  32. Pike TW, Blount JD, Lindström J, Metcalfe NB (2010) Dietary carotenoid availability, sexual signalling and functional fertility in sticklebacks. Biol Lett 6:191–193CrossRefPubMedPubMedCentralGoogle Scholar
  33. Poizat G, Rosecchi E, Crivelli AJ (1999) Empirical evidence of a trade-off between reproductive effort and expectation of future reproduction in female three-spined sticklebacks. Proc R Soc Lond B 266:1543–1548CrossRefGoogle Scholar
  34. Réale D, Garant D, Humphries MM, Bergeron P, Careau V, Montiglio PO (2010) Personality and the emergence of the pace-of-life syndrome concept at the population level. Philos Trans R Soc B 365:4051–4063CrossRefGoogle Scholar
  35. Ricklefs RE, Wikelski M (2002) The physiology/life-history nexus. Trends Ecol Evol 17:462–468CrossRefGoogle Scholar
  36. Rowland WJ (1982) The effects of male nuptial coloration on stickleback aggression: a reexamination. Behaviour 80:118–126CrossRefGoogle Scholar
  37. Rowland WJ (1984) The relationships among nuptial coloration, aggression, and courtship of male three-spined sticklebacks, Gasterosteus aculeatus. Can J Zool 62:999–1004CrossRefGoogle Scholar
  38. Schoepf I, Schradin C (2013) Endocrinology of sociality: comparisons between sociable and solitary individuals within the same population of African striped mice. Horm Behav 64:89–94CrossRefPubMedGoogle Scholar
  39. Schradin C, Scantlebury M, Pillay N, König B (2009) Testosterone levels in dominant sociable males are lower than in solitary roamers: physiological differences between three male reproductive tactics in a sociably flexible mammal. Am Nat 173:376–388CrossRefPubMedGoogle Scholar
  40. Sih A, Bell A, Johnson JC (2004) Behavioral syndromes: an ecological and evolutionary overview. Trends Ecol Evol 19:372–378CrossRefPubMedGoogle Scholar
  41. Stamps JA (2007) Growth-mortality tradeoffs and “personality traits” in animals. Ecol Lett 10:355–363CrossRefPubMedGoogle Scholar
  42. Strong RK, Dabbs JM (2000) Testosterone and behavior in normal young children. Personal Individ Differ 28:909–915CrossRefGoogle Scholar
  43. 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 142:1185–1206CrossRefGoogle Scholar
  44. Whittingham MJ, Stephens PA, Bradbury RB, Freckleton RP (2006) Why do we still use stepwise modelling in ecology and behaviour? J Anim Ecol 75:1182–1189CrossRefPubMedGoogle Scholar
  45. Wilson AD, Godin J-GJ, Ward AJ (2010) Boldness and reproductive fitness correlates in the eastern mosquitofish, Gambusia holbrooki. Ethology 116:96–104CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  1. 1.Departamento de Ecoloxía e Bioloxía AnimalUniversidade de VigoVigoSpain

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