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Correlations begin at home: drivers of co-occurrence patterns in personality and cognitive ability in wild populations of zebrafish

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Abstract

Aquatic habitats are extremely dynamic, with constantly changing ecological factors, which has now been exacerbated due to human-induced rapid environmental change. In such variable environments, it becomes essential to understand how personality and cognition in organisms affect the adaptability of individuals to different habitat conditions. To test this, we studied how personality-related traits as well as cognitive ability differ between populations of wild-caught zebrafish (Danio rerio) from habitats that differed in various environmental factors. We measured emergence into a novel environment as an indicator of boldness, and performance in a spatial task inferred from feeding latencies in a maze over repeated trials to assess learning and memory, as an indicator of cognitive ability. We found that personality affects cognition and although bolder fish are better learners, they show poorer retention of memory across populations. Although personality and cognitive ability varied between habitats, the patterns of their correlations remained similar within each population. However, the individual traits (such as sex and size) that were drivers of personality and cognition differed between the habitats, suggesting that not only do behavioral traits vary between populations, but also the factors that are important in determining them. Personality and cognitive ability and the correlations between these traits determine how well an organism performs in its habitat, as well as how likely it is to find new habitats and adapt to them. Studying these across wild zebrafish populations helps predict performance efficiencies among individuals and also explains how fish adapt to extremely dynamic environments that can lead to variation in behavioral traits and correlations between them. This study not only sheds light on the drivers of interindividual variation and co-occurrence patterns of personality and cognition, but also individual and population factors that might have an effect on them.

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Data obtained from observations will be made available by the authors on request to the corresponding author.

References

  • Arunachalam M, Raja M, Vijayakumar C, Malaiammal P, Mayden RL (2013) Natural history of zebrafish (Danio rerio) in India. Zebrafish 10(1):1–14

    Article  PubMed  Google Scholar 

  • Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67(1):1–48

    Article  Google Scholar 

  • Bengston SE, Dornhaus A (2014) Be meek or be bold? a colony-level behavioural syndrome in ants. Proceed Royal Soc B Biol Sci 281(1791):20140518

    CAS  Google Scholar 

  • Bhat A, Greulich MM, Martins EP (2015) Behavioral plasticity in response to environmental manipulation among zebrafish (Danio rerio) populations. PLoS ONE 10(4):e0125097

    Article  PubMed  PubMed Central  Google Scholar 

  • Bókony V, Kulcsár A, Tóth Z, Liker A (2012) Personality traits and behavioral syndromes in differently urbanized populations of house sparrows (Passer domesticus). PLoS ONE 7(5):e36639

    Article  PubMed  PubMed Central  Google Scholar 

  • Brashares JS, Arcese P (2002) Role of forage, habitat and predation in the behavioural plasticity of a small African antelope. J Anim Ecol 71:626–638

    Article  Google Scholar 

  • Briffa M, Weiss A (2010) Animal personality. Curr Biol 20(21):R912–R914

    Article  CAS  PubMed  Google Scholar 

  • Brust V, Guenther A (2017) Stability of the guinea pigs personality–cognition–linkage over time. Behav Proc 134:4–11

    Article  Google Scholar 

  • Carbia PS, Brown C (2019) Environmental enrichment influences spatial learning ability in captive-reared intertidal gobies (Bathygobius cocosensis). Anim Cogn 22(1):89–98

    Article  PubMed  Google Scholar 

  • Carere C, Locurto C (2011) Interaction between animal personality and animal cognition. Curr Zool 57(4):491–498

    Article  Google Scholar 

  • Colléter M, Brown C (2011) Personality traits predict hierarchy rank in male rainbowfish social groups. Anim Behav 81(6):1231–1237

    Article  Google Scholar 

  • Dadda M, Domenichini A, Piffer L, Argenton F, Bisazza A (2010) Early differences in epithalamic left–right asymmetry influence lateralization and personality of adult zebrafish. Behav Brain Res 206(2):208–215

    Article  PubMed  Google Scholar 

  • Dall SR, Griffith SC (2014) An empiricist guide to animal personality variation in ecology and evolution. Front Ecol Evol 2:3

    Article  Google Scholar 

  • Daniel DK, Bhat A (2020) Bolder and Brighter? Exploring correlations between personality and cognitive abilities among individuals within a population of wild zebrafish Danio Rerio. Front Behav Neurosci 14:138

    Article  PubMed  PubMed Central  Google Scholar 

  • Daniel DK, Bhat A (2022) Sex and population drive interindividual variations in a cognitive task across three populations of wild zebrafish. Front Psychol. https://doi.org/10.3389/fpsyg.2022.786486

    Article  PubMed  PubMed Central  Google Scholar 

  • Del Giudice M (2012) Sex ratio dynamics and fluctuating selection on personality. J Theor Biol 297:48–60

    Article  PubMed  Google Scholar 

  • Delignette-Muller ML, Dutang C (2015) fitdistrplus: An R package for fitting distributions. J Stat Softw 64(4):1–34

    Article  Google Scholar 

  • DePasquale C, Fettrow S, Sturgill J, Braithwaite VA (2019) The impact of flow and physical enrichment onpreferences in zebrafish. Appl Ani Behav Sci 215:77–81

    Article  Google Scholar 

  • Dingemanse NJ, Réale D (2005) Natural selection and animal personality. Behaviour 142:1159–1184

    Article  Google Scholar 

  • Dingemanse NJ, Wright J, Kazem AJ, Thomas DK, Hickling R, Dawnay N (2007) Behavioural syndromes differ predictably between 12 populations of three-spined stickleback. J Anim Ecol 76(6):1128–1138

    Article  PubMed  Google Scholar 

  • Dosmann A, Mateo JM (2014) Food, sex and predators: animal personality persists with multidimensional plasticity across complex environments. Anim Behav 90:109–116

    Article  Google Scholar 

  • Dougherty LR, Guillette LM (2018) Linking personality and cognition: a meta-analysis. Phil Trans R Soc B Biol Sci 373(1756):20170282

    Article  Google Scholar 

  • Downes SJ, Adams M (2001) Geographic variation in antisnake tactics: the evolution of scent-mediated behavior in a lizard. Evolution 55(3):605–615

    Article  CAS  PubMed  Google Scholar 

  • Dubuc-Messier G, Réale D, Perret P, Charmantier A (2017) Environmental heterogeneity and population differences in blue tits personality traits. Behav Ecol 28(2):448–459

    PubMed  Google Scholar 

  • Eggers DM (1982) Planktivore preference by prey size. Ecology 63(2):381–390

    Article  Google Scholar 

  • Engeszer RE, Patterson LB, Rao AA, Parichy DM (2007) Zebrafish in the wild: a review of natural history and new notes from the field. Zebrafish 4(1):21–40

    Article  PubMed  Google Scholar 

  • Evans J, Boudreau K, Hyman J (2010) Behavioural syndromes in urban and rural populations of song sparrows. Ethology 116(7):588–595

    Google Scholar 

  • Foster SA (1995) Understanding the evolution of behavior in threespine stickleback: the value of geographic variation. Behaviour 132(15–16):1107–1129

    Article  Google Scholar 

  • Garnham L, Løvlie H (2018) Sophisticated fowl: the complex behaviour and cognitive skills of chickens and red junglefowl. Behav Sci 8(1):13

    Article  PubMed  PubMed Central  Google Scholar 

  • Garnham LC, Porthén SA, Child S, Forslind S, Løvlie H (2019) The role of personality, cognition, and affective state in same-sex contests in the red junglefowl. Behav Ecol Sociobiol 73(11):1–12

    Article  Google Scholar 

  • Gill AB, Hart PJ (1994) Feeding behaviour and prey choice of the threespine stickleback: the interacting effects of prey size, fish size and stomach fullness. Anim Behav 47(4):921–932

    Article  Google Scholar 

  • Griffin AS, Guillette LM, Healy SD (2015) Cognition and personality: an analysis of an emerging field. Trends Ecol Evol 30(4):207–214

    Article  PubMed  Google Scholar 

  • Guenther A, Brust V, Dersen M, Trillmich F (2014) Learning and personality types are related in cavies (Cavia aperea). J Comp Psychol 128(1):74

    Article  PubMed  Google Scholar 

  • Guillette LM, Naguib M, Griffin AS (2017) Individual differences in cognition and personality. Behav Process 134:1–3

    Article  Google Scholar 

  • Hannunen S, Ekbom B (2002) Within species variation in host plant quality and movement behavior of Lygus rugulipennis nymphs. Entomol Exp Appl 104(1):95–101

    Article  CAS  Google Scholar 

  • Head ML, Lindholm AK, Brooks R (2008) Operational sex ratio and density do not affect directional selection on male sexual ornaments and behavior. Evol Int J Org Evol 62(1):135–144

    Article  Google Scholar 

  • Hopper LM, Price SA, Freeman HD, Lambeth SP, Schapiro SJ, Kendal RL (2014) Influence of personality, age, sex, and estrous state on chimpanzee problem-solving success. Anim Cogn 17(4):835–847

    Article  PubMed  Google Scholar 

  • Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biom J 50(3):346–363

    Article  PubMed  Google Scholar 

  • Hutchings JA, Morris DW (1985) The influence of phylogeny, size and behaviour on patterns of covariation in salmonid life histories. Oikos 45:118–124

    Article  Google Scholar 

  • Irving E, Brown C (2013) Examining the link between personality and laterality in a feral guppy Poecilia reticulata population. J Fish Biol 83(2):311–325

    Article  CAS  PubMed  Google Scholar 

  • Jayakody S, Sibbald AM, Gordon IJ, Lambin X (2008) Red deer Cervus elephus vigilance behaviour differs with habitat and type of human disturbance. Wildl Biol 14(1):81–91

    Article  Google Scholar 

  • Jenouvrier S, Caswell H, Barbraud C, Weimerskirch H (2010) Mating behavior, population growth, and the operational sex ratio: a periodic two-sex model approach. Am Nat 175(6):739–752

    Article  PubMed  Google Scholar 

  • Kareklas K, Elwood RW, Holland RA (2017) Personality effects on spatial learning: comparisons between visual conditions in a weakly electric fish. Ethology 123(8):551–559

    Article  Google Scholar 

  • Kelly JR, Shelton SG, Daniel DK, Bhat A, Mondal R, Nipple F, Shelton DS (2021) Wild zebrafish sentinels: biological monitoring of site differences using behavior and morphology. Toxics 9(7):165

    Article  PubMed  PubMed Central  Google Scholar 

  • Ketterson ED (1979) Aggressive behavior in wintering dark-eyed juncos: determinants of dominance and their possible relation to geographic variation in sex ratio. Wilson Bull 91:371–383

    Google Scholar 

  • King JE (2007) Dimensions of the ape mind: adding personality to behavior and cognition. In: Washburn DA (ed) Primate perspectives on behavior and cognition. American Psychological Association, pp 47–60

    Chapter  Google Scholar 

  • Kralj-Fišer S, Hebets EA, Kuntner M (2017) Different patterns of behavioral variation across and within species of spiders with differing degrees of urbanization. Behav Ecol Sociobiol 71(8):1–15

    Article  Google Scholar 

  • Kroodsma DE, Byers BE, Halkin SL, Hill C, Minis D, Bolsinger JR, Wilda K (1999) Geographic variation in black-capped chickadee songs and singing behavior. Auk 116(2):387–402

    Article  Google Scholar 

  • Kuznetsova A, Brockhoff PB, Christensen RHB (2017) lmerTest package: tests in linear mixed effects models. J Stat Softw 82(13):1–26

    Article  Google Scholar 

  • Liu M, Liu Y, Wang H, Jia J, Liu K (2022) Color discrimination provides insight into the relationship between personality cognition and brain morphology in the western mosquitofish (Gambusia affinis). Brain Behav Evol 97:274–283

    Article  PubMed  Google Scholar 

  • Locurto C (2007) Individual differences and animal personality. Comparat Cogn Behav Rev 2(1):67–78

    Google Scholar 

  • Lucon-Xiccato T, Dadda M (2017) Personality and cognition: sociability negatively predicts shoal size discrimination performance in guppies. Front Psychol 8:1118

    Article  PubMed  PubMed Central  Google Scholar 

  • Lucon-Xiccato T, Montalbano G, Bertolucci C (2020a) Personality traits covary with individual differences in inhibitory abilities in 2 species of fish. Curr Zool 66(2):187–195

    Article  PubMed  Google Scholar 

  • Lucon-Xiccato T, Montalbano G, Dadda M, Bertolucci C (2020b) Lateralization correlates with individual differences in inhibitory control in zebrafish. Biol Let 16(8):20200296

    Article  Google Scholar 

  • Magurran AE (1999) The causes and consequences of geographic variation in antipredator behavior: perspectives from fish populations. In: Margurran AE (ed) Geographic variation in behavior. Oxford University Press, UK

    Google Scholar 

  • Martins EP, Bhat A (2014) Population-level personalities in zebrafish: aggression-boldness across but not within populations. Behav Ecol 25(2):368–373

    Article  Google Scholar 

  • Mayer M, Shine R, Brown GP (2016) Bigger babies are bolder: effects of body size on personality of hatchling snakes. Behaviour 153(3):313–323

    Article  Google Scholar 

  • Medina-García A, Jawor JM, Wright TF (2017) Cognition, personality, and stress in budgerigars Melopsittacus Undulatus. Behav Ecol 28(6):1504–1516

    Article  PubMed  PubMed Central  Google Scholar 

  • Michelangeli M, Cote J, Chapple DG, Sih A, Brodin T, Fogarty S, Wong BB (2020) Sex-dependent personality in two invasive species of mosquitofish. Biol Invasions 22(4):1353–1364

    Article  Google Scholar 

  • Miletto Petrazzini ME, Pecunioso A, Dadda M, Agrillo C (2019) the impact of brain lateralization and anxiety-like behaviour in an extensive operant conditioning task in zebrafish (Danio rerio). Symmetry 11(11):1395

    Article  Google Scholar 

  • Moura RR, Peixoto PEC (2013) The effect of operational sex ratio on the opportunity for sexual selection: a meta-analysis. Anim Behav 86(4):675–683

    Article  Google Scholar 

  • Naguib M, Flörcke C, van Oers K (2011) Effects of social conditions during early development on stress response and personality traits in great tits (Parus major). Dev Psychobiol 53(6):592–600

    Article  PubMed  Google Scholar 

  • Niemelä PT, Vainikka A, Forsman JT, Loukola OJ, Kortet R (2013) How does variation in the environment and individual cognition explain the existence of consistent behavioral differences? Ecol Evol 3(2):457–464

    Article  PubMed  Google Scholar 

  • Parichy DM (2015) The natural history of model organisms: Advancing biology through a deeper understanding of zebrafish ecology and evolution. Elife 4:e05635

    Article  PubMed  PubMed Central  Google Scholar 

  • Parkos JJ III, Wahl DH (2010) Influence of body size and prey type on the willingness of age-0 fish to forage under predation risk. Trans Am Fish Soc 139(4):969–975

    Article  Google Scholar 

  • Quinn JL, Cresswell W (2005) Personality, anti-predation behaviour and behavioural plasticity in the chaffinch Fringilla coelebs. Behaviour 142:1377–1402

    Article  Google Scholar 

  • R Core Team (2021) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria

    Google Scholar 

  • Roy T, Bhat A (2016) Learning and memory in juvenile zebrafish: what makes the difference–population or rearing environment? Ethology 122(4):308–318

    Article  Google Scholar 

  • Roy T, Bhat A (2017) Social learning in a maze? contrasting individual performance among wild zebrafish when associated with trained and naïve conspecifics. Behav Proc 144:51–57

    Article  Google Scholar 

  • Roy T, Bhat A (2018a) Repeatability in boldness and aggression among wild zebrafish (Danio rerio) from two differing predation and flow regimes. J Comp Psychol 132(4):349

    Article  PubMed  Google Scholar 

  • Roy T, Bhat A (2018b) Population, sex and body size: determinants of behavioural variations and behavioural correlations among wild zebrafish Danio rerio. R Soc Open Sci 5(1):170978

    Article  PubMed  PubMed Central  Google Scholar 

  • Roy T, Shukla R, Bhat A (2017) Risk-taking during feeding: between-and within-population variation and repeatability across contexts among wild zebrafish. Zebrafish 14(5):393–403

    Article  PubMed  Google Scholar 

  • Savaşçı BB, Lucon-Xiccato T, Bisazza A (2021) Ontogeny and personality affect inhibitory control in guppies, Poecilia reticulata. Anim Behav 180:111–121

    Article  Google Scholar 

  • Schuett W, Dall SR (2009) Sex differences, social context and personality in zebra finches Taeniopygia Guttata. Anim Behav 77(5):1041–1050

    Article  Google Scholar 

  • Seghers BH (1974) Geographic variation in the responses of guppies (Poecilia reticulata) to aerial predators. Oecologia 14(1):93–98

    Article  CAS  PubMed  Google Scholar 

  • Shelton DS, Shelton SG, Daniel DK, Raja M, Bhat A, Tanguay RL, Martins EP (2020) Collective behavior in wild zebrafish. Zebrafish 17(4):243–252

    Article  PubMed  PubMed Central  Google Scholar 

  • Shukla R, Bhat A (2017) Morphological divergences and ecological correlates among wild populations of zebrafish (Danio rerio). Environ Biol Fishes 100(3):251–264

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Spence R, Magurran AE, Smith C (2011) Spatial cognition in zebrafish: the role of strain and rearing environment. Anim Cogn 14(4):607–612

    Article  PubMed  Google Scholar 

  • Stamps J, Groothuis TG (2010) The development of animal personality: relevance, concepts and perspectives. Biol Rev 85(2):301–325

    Article  PubMed  Google Scholar 

  • Stearns SC (1989) The evolutionary significance of phenotypic plasticity. Bioscience 7:436–445

    Article  Google Scholar 

  • Streit RP, Bellwood DR (2017) High prevalence of homing behaviour among juvenile coral-reef fishes and the role of body size. Coral Reefs 36(4):1083–1095

    Article  Google Scholar 

  • Suriyampola PS, Shelton DS, Shukla R, Roy T, Bhat A, Martins EP (2016) Zebrafish social behavior in the wild. Zebrafish 13(1):1–8

    Article  PubMed  Google Scholar 

  • Wallace KJ, Rausch RT, Ramsey ME, Cummings ME (2020) Sex differences in cognitive performance and style across domains in mosquitofish (Gambusia affinis). Anim Cogn 23(4):655–669

    Article  PubMed  Google Scholar 

  • Weiss A (2018) Personality traits: a view from the animal kingdom. J Pers 86(1):12–22

    Article  PubMed  Google Scholar 

  • White SL, Wagner T, Gowan C, Braithwaite VA (2017) Can personality predict individual differences in brook trout spatial learning ability? Behav Proc 141:220–228

    Article  CAS  Google Scholar 

  • Whiteley AR, Bhat A, Martins EP, Mayden RL, Arunachalam M, Uusi-Heinkkilä SILVA, Bernatchez L (2011) Population genomics of wild and laboratory zebrafish (Danio rerio). Mol Ecol 20(20):4259–4276

    Article  PubMed  PubMed Central  Google Scholar 

  • Wickham H (2016) ggplot2: Elegant graphics for data analysis. Springer-Verlag, New York

    Book  Google Scholar 

  • Wright D, Rimmer LB, Pritchard VL, Butlin RK, Krause J (2003) Inter and intra-population variation in shoaling and boldness in the zebrafish (Danio rerio). J Fish Biol 63:258–259

    Article  Google Scholar 

  • Zidar J, Sorato E, Malmqvist AM, Jansson E, Rosher C, Jensen P, Løvlie H (2017) Early experience affects adult personality in the red junglefowl: a role for cognitive stimulation? Behav Process 134:78–86

    Article  Google Scholar 

  • Zidar J, Balogh A, Favati A, Jensen P, Leimar O, Sorato E, Løvlie H (2018) The relationship between learning speed and personality is age-and task-dependent in red junglefowl. Behav Ecol Sociobiol 72(10):1–13

    Article  Google Scholar 

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Acknowledgements

The authors would like to thank the Indian Institute of Science Education and Research Kolkata, (IISER Kolkata), India for providing infrastructural support, and Council for Science and Industrial Research (CSIR), Government of India, for providing a Senior Research Fellowship to DKD. Authors also thank Mr. Prasenjit Pan for collection of wild zebrafish populations from different habitats, and all members of the Fish Ecology and Behaviour Lab, IISER Kolkata, for lab and population maintenance.

Funding

AB received institutional financial support in the form of Academic Research Funds from Indian Institute of Science Kolkata (India). DKD was funded through a junior and senior research fellowship from the Council of Science and Industrial Research (CSIR), Government of India.

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DKD and AB conceived the goals and the design of the study. DKD conducted the experimental assays, analyzed the videos, performed the statistical analyses and wrote the first draft of the manuscript. AB procured funding and supervised the project. DKD and AB wrote and edited the final version of manuscript. All authors read and approved the submitted version.

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Correspondence to Anuradha Bhat.

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The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

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Guidelines outlined by the Committee for the Purpose of Control and Supervision of Experiments on Animals (CPCSEA), Ministry of Fisheries, Animal Husbandry and Dairying, Government of India were followed in all aspects of maintenance and experimentation. All experimental protocols followed here have been approved by the Institutional Animal Ethics Committee's (IAEC) and guidelines of Indian Institute of Science Education and Research (IISER) Kolkata, Government of India (Approval number IISERK/IAEC/AP/2021/70).

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Daniel, D.K., Bhat, A. Correlations begin at home: drivers of co-occurrence patterns in personality and cognitive ability in wild populations of zebrafish. Anim Cogn 26, 1381–1394 (2023). https://doi.org/10.1007/s10071-023-01787-w

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