Behavioral Ecology and Sociobiology

, Volume 70, Issue 12, pp 2027–2037 | Cite as

Emergence and development of personality over the ontogeny of fish in absence of environmental stress factors

  • Giovanni Polverino
  • Claudia Cigliano
  • Shinnosuke Nakayama
  • Thomas Mehner
Original Article


Animals typically display among-individual differences in behavior that are consistent over time (i.e., personality). These differences are often triggered by variable individual responses to environmental stress factors experienced during life, such as competition for resources and risk of predation. While the causes underlying animal personality are considered to be an issue of prime importance, it is still unknown whether personality emerges and develops over ontogeny if the main sources of behavioral differentiation are absent. Here, we tested whether personality emerged and was strengthened during the lifetime of Eastern mosquitofish (Gambusia holbrooki), once intraspecific competition and risk of predation were completely removed and genetic and maternal differences minimized. We found that individual differences in behavior were overall repeatable over ontogeny (i.e., personality was manifested). Personality was, however, not detectable in juvenile individuals but emerged during and after their sexual maturation. The emergence of personality was triggered by the decline in behavioral plasticity of individuals over ontogeny, while differences in behavior among individuals did not vary with age. Our results suggest that animal personality might be inevitable and emerge in fish under laboratory-controlled conditions even in absence of extrinsic factors that typically lead to behavioral differentiation. The decline of behavioral plasticity over lifetime might be a relevant mechanism for the development of personality in animals.

Significance statement

Increasing evidence suggests that animals have personality, that is, individuals consistently differ in behavior among each other (e.g., bold and shy or social and non-social individuals). Personality differences among animals should be, by definition, consistent over time and often caused by environmental challenges experienced early in life. In this study, we observed that personality differences were not present at juvenile age in social fish but emerged later in their life, despite the fact that environmental challenges (i.e., predation risk and competition for space, food, and mates) were absent. Personality differences strengthened over lifetime, resulting from declines in individual behavioral plasticity. Our results suggest that the decline in behavioral plasticity with age may represent a relevant mechanism for behavioral differentiation in animals, in agreement with evidences from the human literature on age-related loss in behavioral plasticity.


Behavioral type Developmental plasticity Lifetime Gambusia Repeatability Temperament 



The authors would like to acknowledge K. Kuntze, T. Ruberto, and N. Gamrath for the help provided with the laboratory procedures and F. Del Sette for the support to realize Fig. 1a. We also thank all members of the B-Types group for providing important feedbacks during all phases of the study and the research group Evolutionary Ecology of Variation for the statistical support. A further acknowledgement goes to all participants to the workshop “New perspectives in behavioral development: adaptive shaping of behavior over a lifetime?” at the Center for Interdisciplinary Research (ZiF), Bielefeld University, Bielefeld (Germany), for the fundamental insights that contributed to the realization of this study.

Compliance with ethical standards


This work was part of the B-Types project ( funded through the Wissenschaftsgemeinschaft Leibniz (WGL, SAW-2013-IGB-2).

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. The experimental procedure was approved through an animal care permit (G 0074/15) granted by the Landesamt für Gesundheit und Soziales Berlin (LAGeSo). Both housing and experimental procedures were designed to minimize stress in the tested animals.

Informed consent

Informed consent was obtained from all individual participants included in the study.

Supplementary material

265_2016_2206_MOESM1_ESM.docx (1.5 mb)
ESM 1 (DOCX 1541 kb)


  1. Ariani AP, Camassa MM, Wittmann KJ (2000) The dolinas of Torre Castiglione (Gulf of Tarent, Italy): environmental and faunistic aspects of a semi-hypogean water system. Mem Biospeol 27:1–14Google Scholar
  2. Arnold C, Taborsky B (2010) Social experience in early ontogeny has lasting effects on social skills in cooperatively breeding cichlids. Anim Behav 79:621–630CrossRefGoogle Scholar
  3. Ayroles JF, Buchanan SM, O’Leary C, Skutt-Kakaria K, Grenier JK, Clark AG, Hartl DL, de Bivort BL (2015) Behavioral idiosyncrasy reveals genetic control of phenotypic variability. P Natl Acad Sci USA 112:6706–6711CrossRefGoogle Scholar
  4. Baltes PB (1997) On the incomplete architecture of human ontogeny: selection, optimization, and compensation as foundation of developmental theory. Am Psychol 52:366–380CrossRefPubMedGoogle Scholar
  5. Baltes PB, Baltes MM (1993) Successful aging: perspectives from the behavioral sciences, vol 4. Cambridge University Press, CambridgeGoogle Scholar
  6. Bates D, Maechler M, Bolker B, Walker S (2014) lme4: linear mixed-effects models using Eigen and S4. R package version 1.1–5,
  7. Bell AM, Hankison SJ, Laskowski KL (2009) The repeatability of behaviour: a meta-analysis. Anim Behav 77:771–783CrossRefPubMedPubMedCentralGoogle Scholar
  8. Bell AM, McGhee KE, Stein LR (2016) Effects of mothers’ and fathers’ experience with predation risk on the behavioral development of their offspring in threespined sticklebacks. Curr Opin Behav Sci 7:28–32CrossRefPubMedGoogle Scholar
  9. Bestion E, Teyssier A, Aubret F, Clobert J, Cote J (2014) Maternal exposure to predator scents: offspring phenotypic adjustment and dispersal. Proc R Soc B 281:–20140701Google Scholar
  10. Biro PA, Stamps JA (2008) Are animal personality traits linked to life-history productivity? Trends Ecol Evol 23:361–368CrossRefPubMedGoogle Scholar
  11. 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
  12. Biro PA, Stamps JA (2015) Using repeatability to study physiological and behavioural traits: ignore time-related change at your peril. Anim Behav 105:223–230CrossRefGoogle Scholar
  13. Bisazza A (1993) Male competition, female mate choice and sexual size dimorphism in poeciliid fishes. Mar Freshw Behav Phy 23:257–286CrossRefGoogle Scholar
  14. Brommer JE, Class B (2015) The importance of genotype-by-age interactions for the development of repeatable behavior and correlated behaviors over lifetime. Front Zool 12:S2CrossRefPubMedPubMedCentralGoogle Scholar
  15. Brooks S, Tyler CR, Sumpter JP (1997) Egg quality in fish: what makes a good egg? Rev Fish Biol Fish 7:387–416CrossRefGoogle Scholar
  16. Carere C, Drent PJ, Koolhaas JM, Groothuis TG (2005) Epigenetic effects on personality traits: early food provisioning and sibling competition. Behaviour 142:1329–1355CrossRefGoogle Scholar
  17. Dadda M, Pilastro A, Bisazza A (2005) Male sexual harassment and female schooling behavior in the eastern mosquitofish. Anim Behav 70:463–471CrossRefGoogle Scholar
  18. Dingemanse NJ, Dochtermann NA (2013) Quantifying individual variation in behaviour: mixed-effect modelling approaches. J Anim Ecol 82:39–54CrossRefPubMedGoogle Scholar
  19. DiRienzo N, Pruitt JN, Hedrick AV (2012) Juvenile exposure to acoustic sexual signals from conspecifics alters growth trajectory and an adult personality trait. Anim Behav 84:861–868CrossRefGoogle Scholar
  20. Dochtermann NA, Schwab T, Sih A (2015) The contribution of additive genetic variation to personality variation: heritability of personality. Proc R Soc B 282:20142201CrossRefPubMedPubMedCentralGoogle Scholar
  21. Drent PJ, van Oers K, van Noordwijk AJ (2003) Realized heritability of personalities in the great tit (Parus major). Proc R Soc Lond B 270:45–51CrossRefGoogle Scholar
  22. Earley RL, Edwards JT, Aseem O, Felton K, Blumer LS, Karom M, Grober MS (2006) Social interactions tune aggression and stress responsiveness in a territorial cichlid fish (Archocentrus nigrofasciatus). Physiol Behav 88:353–363CrossRefPubMedGoogle Scholar
  23. Edenbrow M, Croft DP (2013) Environmental and genetic effects shape the development of personality traits in the mangrove killifish Kryptolebias marmoratus. Oikos 122:667–681CrossRefGoogle Scholar
  24. Favati A, Zidar J, Thorpe H, Jensen P, Løvlie H (2015) The ontogeny of personality traits in the red junglefowl, Gallus gallus. Behav Ecol 27:484–493CrossRefGoogle Scholar
  25. Fawcett TW, Frankenhuis WE (2015) Adaptive explanations for sensitive windows in development. Front Zool 12:1–14CrossRefGoogle Scholar
  26. Fernández-Delgado C, Rossomanno S (1997) Reproductive biology of the mosquitofish in a permanent natural lagoon in south-west Spain: two tactics for one species. J Fish Biol 51:80–92CrossRefPubMedGoogle Scholar
  27. Fischer B, van Doorn GS, Dieckmann U, Taborsky B (2014) The evolution of age-dependent plasticity. Am Nat 183:108–125CrossRefPubMedGoogle Scholar
  28. Fisher DN, David M, Tregenza T, Rodríguez-Muñoz R (2015) Dynamics of among-individual behavioral variation over adult lifespan in a wild insect. Behav Ecol 26:975–985CrossRefPubMedPubMedCentralGoogle Scholar
  29. Frederick JL (1997) Evaluation of fluorescent elastomer injection as a method for marking small fish. Bull Mar Sci 61:399–408Google Scholar
  30. Freund J, Brandmaier AM, Lewejohann L, Kirste I, Kritzler M, Krüger A, Sachser N, Lindenberger U, Kempermann G (2013) Emergence of individuality in genetically identical mice. Science 340:756–775CrossRefPubMedGoogle Scholar
  31. Froese R (2006) Cube law, condition factor and weight–length relationships: history, meta-analysis and recommendations. J Appl Ichthyol 22:241–253CrossRefGoogle Scholar
  32. Gorski JN, Dunn-Meynell AA, Hartman TG, Levin BE (2006) Postnatal environment overrides genetic and prenatal factors influencing offspring obesity and insulin resistance. Am J Physiol-Reg I 291:R768–R778Google Scholar
  33. Gosling SD (2001) From mice to men: what can we learn about personality from animal research? Psychol Bull 127:45CrossRefPubMedGoogle Scholar
  34. Haake PW, Dean JM (1983) Age and growth of four Everglades fishes using otolith techniques. Technical Report SFRC83/03 South Florida Research Center, Everglades National Park Homestead, FLGoogle Scholar
  35. Hadfield JD (2010) MCMC methods for multi-response generalized linear mixed models: the MCMCglmm R package. J Stat Softw 33:1–22CrossRefGoogle Scholar
  36. Halperin JRP, Dunham DW, Ye S (1992) Social isolation increases social display after priming in Betta splendens but decreases aggressive readiness. Behav Process 28:13–31CrossRefGoogle Scholar
  37. Han CS, Brooks RC (2015) The interaction between genotype and juvenile and adult density environment in shaping multidimensional reaction norms of behaviour. Funct Ecol 29:78–87CrossRefGoogle Scholar
  38. Hannes RP, Franck D (1983) The effect of social isolation on androgen and corticosteroid levels in a cichlid fish (Haplochromis burtoni) and in swordtails (Xiphophorus helleri). Horm Behav 17:292–301CrossRefPubMedGoogle Scholar
  39. Herborn KA, Macleod R, Miles WT, Schofield AN, Alexander L, Arnold KE (2010) Personality in captivity reflects personality in the wild. Anim Behav 79:835–843CrossRefGoogle Scholar
  40. Kain JS, Stokes C, de Bivort BL (2012) Phototactic personality in fruit flies and its suppression by serotonin and white. P Natl Acad Sci USA 109:19834–19839CrossRefGoogle Scholar
  41. Killen SS, Marras S, Metcalfe NB, McKenzie DJ, Domenici P (2013) Environmental stressors alter relationships between physiology and behaviour. Trends Ecol Evol 28:651–658CrossRefPubMedGoogle Scholar
  42. Krause J, Loader SP, McDermott J, Ruxton GD (1998) Refuge use by fish as a function of body length–related metabolic expenditure and predation risks. Proc R Soc Lond B 265:2373–2379CrossRefGoogle Scholar
  43. Kuznetsova A, Brockhoff PB, Christensen RHB (2016) lmerTest: tests in linear mixed effect models. R package version 2–6,
  44. Laskowski KL, Pruitt JN (2014) Evidence of social niche construction: persistent and repeated social interactions generate stronger personalities in a social spider. Proc R Soc B 281:20133166CrossRefPubMedPubMedCentralGoogle Scholar
  45. Laskowski KL, Montiglio PO, Pruitt JN (2016) Individual and group performance suffers from social niche disruption. Am Nat 187:776–785CrossRefPubMedGoogle Scholar
  46. Matthews SA, Wong MY (2015) Temperature-dependent resolution of conflict over rank within a size-based dominance hierarchy. Behav Ecol 26:947–958CrossRefGoogle Scholar
  47. Nakagawa S, Schielzeth H (2010) Repeatability for Gaussian and non-Gaussian data: a practical guide for biologists. Biol Rev 85:935–956PubMedGoogle Scholar
  48. Nettle D, Bateson M (2015) Adaptive developmental plasticity: what is it, how can we recognize it and when can it evolve? Proc R Soc B 282:20151005CrossRefPubMedPubMedCentralGoogle Scholar
  49. Nilsson PA, Brönmark C (2000) Prey vulnerability to a gape-size limited predator: behavioural and morphological impacts on northern pike piscivory. Oikos 88:539–546CrossRefGoogle Scholar
  50. Oliveira RF, Almada VC, Canario AV (1996) Social modulation of sex steroid concentrations in the urine of male cichlid fish Oreochromis mossambicus. Horm Behav 30:2–12CrossRefPubMedGoogle Scholar
  51. Pinheiro J, Bates D, DebRoy S, Sarkar D, R Core Team (2014) nlme: linear and nonlinear mixed effects models. R package version 3.1–118,
  52. Polverino G, Liao JC, Porfiri M (2013) Mosquitofish (Gambusia affinis) preference and behavioral response to animated images of conspecifics altered in their color, aspect ratio, and swimming depth. PLoS One 8:e54315CrossRefPubMedPubMedCentralGoogle Scholar
  53. Polverino G, Ruberto T, Staaks G, Mehner T (2016) Tank size alters mean behaviours and individual rank orders in personality traits of fish depending on their life stage. Anim Behav 115:127–135CrossRefGoogle Scholar
  54. Pyke GH (2005) A review of the biology of Gambusia affinis and G. holbrooki. Rev Fish Biol Fish 15:339–365CrossRefGoogle Scholar
  55. R Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria, /
  56. Réale D, Reader SM, Sol D, McDougall PT, Dingemanse NJ (2007) Integrating animal temperament within ecology and evolution. Biol Rev 82:291–318CrossRefPubMedGoogle Scholar
  57. Reddon AR (2011) Parental effects on animal personality. Behav Ecol 23:242–245CrossRefGoogle Scholar
  58. Rittschof CC, Bukhari SA, Sloofman LG, et al. (2014) Neuromolecular responses to social challenge: common mechanisms across mouse, stickleback fish, and honey bee. P Natl Acad Sci USA 111:17929–17934CrossRefGoogle Scholar
  59. Seeman TE, McEwen BS (1996) Impact of social environment characteristics on neuroendocrine regulation. Psychosom Med 58:459–471CrossRefPubMedGoogle Scholar
  60. Senner NR, Conklin JR, Piersma T (2015) An ontogenetic perspective on individual differences. Proc R Soc B 282:20151050CrossRefPubMedPubMedCentralGoogle Scholar
  61. Sih A, Mathot KJ, Moiron M, Montiglio PO, Wolf M, Dingemanse NJ (2015) Animal personality and state–behaviour feedbacks: a review and guide for empiricists. Trends Ecol Evol 30:50–60CrossRefPubMedGoogle Scholar
  62. Sogard SM (1997) Size-selective mortality in the juvenile stage of teleost fishes: a review. Bull Mar Sci 60:1129–1157Google Scholar
  63. Stamps JA, Krishnan VV (2014) Combining information from ancestors and personal experiences to predict individual differences in developmental trajectories. Am Nat 184:647–657CrossRefPubMedGoogle Scholar
  64. Stearns SC (1989) The evolutionary significance of phenotypic plasticity. Bioscience 39:436–445CrossRefGoogle Scholar
  65. Trillmich F, Hudson R (2011) The emergence of personality in animals: the need for a developmental approach. Dev Psychobiol 53:505–509CrossRefPubMedGoogle Scholar
  66. Trillmich F, Günther A, Müller C, Reinhold K, Sachser N (2015) New perspectives in behavioural development: adaptive shaping of behaviour over a lifetime? Front Zool 12:S1CrossRefPubMedCentralGoogle Scholar
  67. Turner CL (1941) Morphogenesis of the gonopodium in Gambusia affinis affinis. J Morphol 69:161–185CrossRefGoogle Scholar
  68. Urszán TJ, Garamszegi LZ, Nagy G, Hettyey A, Török J, Herczeg G (2015) No personality without experience? A test on Rana dalmatina tadpoles. Ecol Evol 5:5847–5856CrossRefPubMedPubMedCentralGoogle Scholar
  69. 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
  70. van Overveld T, Matthysen E (2010) Personality predicts spatial responses to food manipulations in free-ranging great tits (Parus major). Biol Lett 6:187–190CrossRefPubMedGoogle Scholar
  71. Ward AJW, Mehner T (2010) Multimodal mixed messages: the use of multiple cues allows greater accuracy in social recognition and predator detection decisions in the mosquitofish, Gambusia holbrooki. Behav Ecol 21:1315–1320CrossRefGoogle Scholar
  72. West-Eberhard MJ (1989) Phenotypic plasticity and the origins of diversity. Annu Rev Ecol Syst 20:249–278CrossRefGoogle Scholar
  73. Wolf M, McNamara JM (2012) On the evolution of personalities via frequency-dependent selection. Am Nat 179:679–692CrossRefPubMedGoogle Scholar
  74. Wolf M, Weissing FJ (2010) An explanatory framework for adaptive personality differences. Philos T Roy Soc B 365:3959–3968CrossRefGoogle Scholar
  75. Wolf M, van Doorn GS, Leimar O, Weissing FJ (2007) Life-history trade-offs favour the evolution of animal personalities. Nature 447:581–584CrossRefPubMedGoogle Scholar
  76. Wong M, Balshine S (2011) Fight for your breeding right: hierarchy re-establishment predicts aggression in a social queue. Biol Lett 7:190–193CrossRefPubMedGoogle Scholar
  77. Wright CM, Holbrook CT, Pruitt JN (2014) Animal personality aligns task specialization and task proficiency in a spider society. P Natl Acad Sci USA 111:9533–9537CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Giovanni Polverino
    • 1
  • Claudia Cigliano
    • 1
  • Shinnosuke Nakayama
    • 1
    • 2
  • Thomas Mehner
    • 1
  1. 1.Department of Biology and Ecology of FishesLeibniz-Institute of Freshwater Ecology and Inland FisheriesBerlinGermany
  2. 2.Division of Integrative Fisheries Management, Faculty of Life SciencesHumboldt Universität zu BerlinBerlinGermany

Personalised recommendations