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

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Abstract

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.

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Acknowledgments

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.

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Authors and Affiliations

  1. Department of Biology and Ecology of Fishes, Leibniz-Institute of Freshwater Ecology and Inland Fisheries, Müggelseedamm 310, 12587, Berlin, Germany

    Giovanni Polverino, Claudia Cigliano, Shinnosuke Nakayama & Thomas Mehner

  2. Division of Integrative Fisheries Management, Faculty of Life Sciences, Humboldt Universität zu Berlin, Berlin, Germany

    Shinnosuke Nakayama

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  1. Giovanni Polverino
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  2. Claudia Cigliano
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  3. Shinnosuke Nakayama
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  4. Thomas Mehner
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Correspondence to Giovanni Polverino.

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Funding

This work was part of the B-Types project (http://www.b-types.igb-berlin.de/) funded through the Wissenschaftsgemeinschaft Leibniz (WGL, SAW-2013-IGB-2).

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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.

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

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Communicated by J. Lindström

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Polverino, G., Cigliano, C., Nakayama, S. et al. Emergence and development of personality over the ontogeny of fish in absence of environmental stress factors. Behav Ecol Sociobiol 70, 2027–2037 (2016). https://doi.org/10.1007/s00265-016-2206-z

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