Age, but not hand preference, is related to personality traits in common marmosets (Callithrix jacchus)
Status PubMed-not-MEDLINE Jazyk angličtina Země Anglie, Velká Británie Médium electronic-ecollection
Typ dokumentu časopisecké články
PubMed
36300134
PubMed Central
PMC9579762
DOI
10.1098/rsos.220797
PII: rsos220797
Knihovny.cz E-zdroje
- Klíčová slova
- behaviour coding, cerebral lateralization, handedness, laterality, temperament,
- Publikační typ
- časopisecké články MeSH
The proximate mechanisms underlying animal personalities, i.e. consistent inter-individual differences in behaviour, are a matter of discussion. Brain lateralization, expressed as the preferred use of the contralateral limb, has been suggested as one of these mechanisms. In this study, we measured a proxy of brain lateralization in captive common marmosets (N = 28) by testing hand preference in a simple food-reaching task and evaluated personality by coding a wide range of behaviours observed in daily situations. We explored the links between personality and both direction and strength of hand preference, as well as age and sex, using linear models. Principal component analysis revealed that the stable behavioural variables were organized in three personality dimensions: Agreeableness, Extraversion and Neuroticism. Regarding hand preference, 14 individuals were left-handed, seven were right-handed and seven were ambilateral. Contrary to our predictions, we did not find any relationship between personality scores and hand preference or sex. Instead, age was a significant predictor of personality scores, with older individuals being more agreeable and less extraverted. The link between brain lateralization and personality seems to be equivocal and dependent on personality and brain lateralization assessment methods. Further examinations of other proximate mechanisms, such as physiology or (epi)genetics, may elucidate what drives personality variation in common marmosets.
Bratislava Zoo Bratislava Slovakia
Department of Zoology Faculty of Science University of South Bohemia České Budějovice Czech Republic
Zobrazit více v PubMed
Norman M, Rowden LJ, Cowlishaw G. 2021. Potential applications of personality assessments to the management of non-human primates: a review of 10 years of study. PeerJ 9, e12044. (10.7717/peerj.12044) PubMed DOI PMC
Wilson V, Guenther A, Øverli Ø, Seltmann MW, Altschul D. 2019. Future directions for personality research: contributing new insights to the understanding of animal behavior. Animals 9, 240. (10.3390/ani9050240) PubMed DOI PMC
Réale D, Reader SM, Sol D, McDougall PT, Dingemanse NJ. 2007. Integrating animal temperament within ecology and evolution. Biol. Rev. 82, 291-318. (10.1111/j.1469-185X.2007.00010.x) PubMed DOI
Stamps J, Groothuis TGG. 2010. The development of animal personality: relevance, concepts and perspectives. Biol. Rev. Camb. Philos. Soc. 85, 301-325. (10.1111/j.1469-185X.2009.00103.x) PubMed DOI
Trillmich F, Müller T, Müller C. 2018. Understanding the evolution of personality requires the study of mechanisms behind the development and life history of personality traits. Biol. Lett. 14, 20170740. (10.1098/rsbl.2017.0740) PubMed DOI PMC
van Oers K, de Jong G, van Noordwijk A, Drent P. 2005. Contribution of genetics to the study of animal personalities: a review of case studies. Behaviour 142, 1185-1206. (10.1163/156853905774539364) DOI
Dochtermann NA, Schwab T, Sih A. 2015. The contribution of additive genetic variation to personality variation: heritability of personality. Proc. R. Soc. B 282, 20142201. (10.1098/rspb.2014.2201) PubMed DOI PMC
Koolhaas JM, Korte SM, De Boer SF, Van Der Vegt BJ, Van Reenen CG, Hopster H, De Jong IC, Ruis MAW, Blokhuis HJ. 1999. Coping styles in animals: current status in behavior and stress- physiology. Neurosci. Biobehav. Rev. 23, 925-935. (10.1016/S0149-7634(99)00026-3) PubMed DOI
Roulin A, Dreiss AN, Kölliker M. 2010. Evolutionary perspective on the interplay between family life, and parent and offspring personality. Ethology 116, 787-796. (10.1111/j.1439-0310.2010.01793.x) DOI
Dammhahn M, Dingemanse NJ, Niemelä PT, Réale D. 2018. Pace-of-life syndromes: a framework for the adaptive integration of behaviour, physiology and life history. Behav. Ecol. Sociobiol. 72, 62. (10.1007/s00265-018-2473-y) DOI
Hinde K, Capitanio JP. 2010. Lactational programming? Mother's milk energy predicts infant behavior and temperament in Rhesus Macaques (Macaca mulatta). Am. J. Primatol. 72, 522-529. (10.1002/ajp.20806) PubMed DOI PMC
Goursot C, Düpjan S, Kanitz E, Tuchscherer A, Puppe B, Leliveld LMC. 2019. Assessing animal individuality: links between personality and laterality in pigs. Curr. Zool. 65, 541-551. (10.1093/cz/zoy071) PubMed DOI PMC
Rogers LJ. 2009. Hand and paw preferences in relation to the lateralized brain. Phil. Trans. R. Soc. B 364, 943-954. (10.1098/rstb.2008.0225) PubMed DOI PMC
Manns M, Basbasse YE, Freund N, Ocklenburg S. 2021. Paw preferences in mice and rats: meta-analysis. Neurosci. Biobehav. Rev. 127, 593-606. (10.1016/j.neubiorev.2021.05.011) PubMed DOI
Barnard S, Wells DL, Hepper PG, Milligan ADS. 2017. Association between lateral bias and personality traits in the domestic dog (Canis familiaris). J. Comp. Psychol. 131, 246-256. (10.1037/com0000074) PubMed DOI
Díaz S, Murray L, Rodway P. 2021. Laterality Limb preference and personality in donkeys (Equus asinus). Laterality Asymmetries Brain, Behav. Cogn. 26, 186-200. (10.1080/1357650X.2021.1882480) PubMed DOI
Caspar KR, Pallasdies F, Mader L, Sartorelli H, Begall S. 2021. The evolution and biological correlates of hand preferences in anthropoid primates. bioRxiv Prepr. (10.1101/2021.12.30.474462) PubMed DOI PMC
Kuběnová B, Lhota S, Tomanová V, Blažek V, Konečná M. 2022. Lion-tailed macaques show a stable direction and reinforcement of hand preference in simple reaching tasks over several years. J. Vertebr. Biol. 71, 21076. (10.25225/jvb.21076) DOI
Reddon AR, Hurd PL. 2009. Individual differences in cerebral lateralization are associated with shy–bold variation in the convict cichlid. Anim. Behav. 77, 189-193. (10.1016/j.anbehav.2008.09.026) DOI
Rogers LJ, Ward JP, Stanford D. 1994. Eye dominance in the small-eared bushbaby, Otolemur garnettii. Neuropsychologia 32, 257-264. (10.1016/0028-3932(94)90011-6) PubMed DOI
Quaranta A, Siniscalchi M, Vallortigara G. 2007. Asymmetric tail-wagging responses by dogs to different emotive stimuli. Curr. Biol. 17, 199-201. (10.1016/j.cub.2007.02.008) PubMed DOI
Byrnes EE, Pouca CV, Chambers SL. 2016. Into the wild: developing field tests to examine the link between elasmobranch personality and laterality. Behaviour 153, 1777-1793. (10.1163/1568539X-00003373) DOI
Niven JE, Frasnelli E. 2018. Insights into the evolution of lateralization from the insects. In Progress in brain research, pp. 3-31. Amsterdam, The Netherlands: Elsevier B.V. PubMed
Vallortigara G, Bisazza A. 2002. How ancient is brain lateralization? In Comparative vertebrate lateralization (eds Rogers LJ, Andrew RJ), pp. 9-69. Cambridge, UK: Cambridge University Press.
Piddington T, Rogers LJ. 2013. Strength of hand preference and dual task performance by common marmosets. Anim. Cogn. 16, 127-135. (10.1007/s10071-012-0562-2) PubMed DOI
Rogers LJ, Zucca P, Vallortigara G. 2004. Advantages of having a lateralized brain. Proc. R. Soc. B 271, 420-422. (10.1098/rsbl.2004.0200) PubMed DOI PMC
Vallortigara G. 2006. The evolutionary psychology of left and right: costs and benefits of lateralization. Dev. Psychobiol. 48, 418-427. (10.1002/dev.20166) PubMed DOI
Rogers LJ. 2021. Brain lateralization and cognitive capacity. Animals 11, 1996. (10.3390/ani11071996) PubMed DOI PMC
Davidson RJ. 1992. Emotion and affective style: hemispheric substrates. Psychol. Sci. 3, 39-43. (10.1111/j.1467-9280.1992.tb00254.x) DOI
Rogers LJ. 2018. Manual bias, behavior, and cognition in common marmosets and other primates. In Progress in brain research, pp. 91-113. Amsterdam, The Netherlands: Elsevier B.V. PubMed
Fernández-Lázaro G, Latorre R, Alonso-García E, Barja Núñez I. 2019. Nonhuman primate welfare: can there be a relationship between personality, lateralization and physiological indicators? Behav. Process. 166, 103897. (10.1016/j.beproc.2019.103897) PubMed DOI
McDowell LJ, Wells DL, Hepper PG, Dempster M. 2016. Lateral bias and temperament in the domestic cat (Felis silvestris). J. Comp. Psychol. 130, 313-320. (10.1037/com0000030) PubMed DOI
Westergaard GC, Chavanne TJ, Lussier ID, Houser L, Cleveland A, Suomi SJ, Higley JD. 2003. Left-handedness is correlated with CSF monoamine metabolite and plasma cortisol concentrations, and with impaired sociality, in free-ranging adult male rhesus macaques (Macaca mulatta). Laterality 8, 169-187. (10.1080/713754484) PubMed DOI
Schneider LA, Delfabbro PH, Burns NR. 2013. Temperament and lateralization in the domestic dog (Canis familiaris). J. Vet. Behav. Clin. Appl. Res. 8, 124-134. (10.1016/j.jveb.2012.06.004) DOI
Grimshaw GM, Wilson MS. 2013. A sinister plot? Facts, beliefs, and stereotypes about the left-handed personality. Laterality 18, 135-151. (10.1080/1357650X.2011.631546) PubMed DOI
Byrnes EE, Vila-Pouca C, Brown C. 2016. Laterality strength is linked to stress reactivity in Port Jackson sharks (Heterodontus portusjacksoni). Behav. Brain Res. 305, 239-246. (10.1016/j.bbr.2016.02.033) PubMed DOI
Westergaard GC, Chavanne TJ, Houser L, Cleveland A, Snoy PJ, Suomi SJ, Highley JD. 2004. Biobehavioural correlates of hand preference in free-ranging female primates. Laterality 9, 267-285. (10.1080/13576500342000086) PubMed DOI
Furnham A. 1983. Personality and handedness. Pers. Individ. Dif. 4, 715-716. (10.1016/0191-8869(83)90132-0) DOI
Reddon AR, Hurd PL. 2008. Aggression, sex and individual differences in cerebral lateralization in a cichlid fish. Biol. Lett. 4, 338-340. (10.1098/rsbl.2008.0206) PubMed DOI PMC
Huber KB, Marsolek CJ. 2022. Do cerebral motivational asymmetries mediate the relationship between handedness and personality? Laterality 27, 21-56. (10.1080/1357650X.2021.1942483) PubMed DOI
Coren S. 1994. Personality differences betwteen left- and right-handers: an overlooked minority group? J. Res. Pers. 28, 214-229. (10.1006/jrpe.1994.1016) DOI
Killgore WDS, Della PL, Casasanto DJ. 1999. Hemispheric laterality and self-rated personality traits. Percept. Mot. Skills 89, 994-996. (10.2466/pms.1999.89.3.994) PubMed DOI
Box HO. 1977. Observations on spontaneous hand use in the common marmoset (Callithrix jacchus). Primates 18, 395-400. (10.1007/BF02383117) DOI
Hook-Costigan MA, Rogers LJ. 1995. Hand, mouth and eye preference in the common marmoset (Callithrix jacchus). Folia Primatol. 64, 180-191. (10.1159/000156851) PubMed DOI
Rothe H. 1973. Handedness in the common marmoset (Callithrix jacchus). Am. J. Phys. Anthropol. 38, 561-565. (10.1002/ajpa.1330380267) PubMed DOI
Cameron R, Rogers LJ. 1999. Hand preference of the common marmoset (Callithrix jacchus): problem solving and responses in a novel setting. J. Comp. Psychol. 113, 149-157. (10.1037/0735-7036.113.2.149) DOI
Malukiewicz J, et al. 2020. An introduction to the callithrix genus and overview of recent advances in marmoset research. ILAR J. 61, 110-138. (10.1093/ilar/ilab027) PubMed DOI
Masilkova M, Boukal D, Ash H, Buchanan-Smith HM, Konečná M. 2022. Linking personality traits and reproductive success in common marmoset (Callithrix jacchus). Sci. Rep. 12, 13341. (10.1038/s41598-022-16339-4) PubMed DOI PMC
Hook MA, Rogers LJ. 2000. Development of hand preferences in marmosets (Callithrix jacchus) and effects of aging. J. Comp. Psychol. 114, 263-271. (10.1037/0735-7036.114.3.263) PubMed DOI
Hook-Costigan MA, Rogers LJ. 1998. Eye preferences in common marmosets (Callithrix jacchus): influence of age, stimulus, and hand preference. Laterality 3, 109-130. (10.1080/713754297) PubMed DOI
Cordeiro de Sousa MB, Xavier NS, Alves da Silva HP, De Oliveira MS, Yamamoto ME. 2001. Hand preference study in marmosets (Callithrix jacchus) using food reaching tests. Primates 42, 57-66. (10.1007/BF02640689) DOI
Hashimoto T, Yamazaki Y, Iriki A. 2013. Hand preference depends on posture in common marmosets. Behav. Brain Res. 248, 144-1150. (10.1016/j.bbr.2013.04.001) PubMed DOI
Vaughan E, Le A, Casey M, Workman KP, Lacreuse A. 2019. Baseline cortisol levels and social behavior differ as a function of handedness in marmosets (Callithrix jacchus). Am. J. Primatol. 81, e23057. (10.1002/ajp.23057) PubMed DOI PMC
Matoba M, Masataka N, Tanioka Y. 1991. Cross-generational continuity of hand-use preferences in marmosets. Behaviour 117, 281-286. (10.1163/156853991X00580) DOI
Tomassetti D, Caracciolo S, Manciocco A, Chiarotti F, Vitale A, De Filippis B. 2019. Personality and lateralization in common marmosets (Callithrix jacchus). Behav. Process. 167, 103899. (10.1016/j.beproc.2019.103899) PubMed DOI
Braccini SN, Caine NG. 2009. Hand preference predicts reactions to novel foods and predators in marmosets (Callithrix geoffroyi). J. Comp. Psychol. 123, 18-25. (10.1037/a0013089) PubMed DOI
Gordon DJ, Rogers LJ. 2010. Differences in social and vocal behavior between left- and right-handed common marmosets (Callithrix jacchus). J. Comp. Psychol. 124, 402-411. (10.1037/a0019736) PubMed DOI
Weiss A, Yokoyama C, Hayashi T, Inoue-Murayama M. 2021. Personality, subjective well-being, and the serotonin 1a receptor gene in common marmosets (Callithrix jacchus). PLoS ONE 16, e0238663. (10.1371/journal.pone.0238663) PubMed DOI PMC
Masilkova M, Weiss A, Šlipogor V, Konečná M. 2020. Comparative assessment of behaviorally derived personality structures in golden-handed Tamarins (Saguinus midas), cotton-top tamarins (Saguinus oedipus), and common marmosets (Callithrix jacchus). J. Comp. Psychol. 134, 453-466. (10.1037/com0000226) PubMed DOI
Šlipogor V, Gunhold-de Oliveira T, Tadić Z, Massen JJM, Bugnyar T. 2016. Consistent inter-individual differences in common marmosets (Callithrix jacchus) in boldness-shyness, stress-activity, and exploration-avoidance. Am. J. Primatol. 78, 961-973. (10.1002/ajp.22566) PubMed DOI PMC
Koski SE, Burkart JM. 2015. Common marmosets show social plasticity and group-level similarity in personality. Sci. Rep. 5, 8878. (10.1038/srep08878) PubMed DOI PMC
Iwanicki S, Lehmann J. 2015. Behavioral and trait rating assessments of personality in common marmosets (Callithrix jacchus). J. Comp. Psychol. 129, 205-217. (10.1037/a0039318) PubMed DOI
Šlipogor V, Massen JJMM, Schiel N, Souto A, Bugnyar T. 2021. Temporal consistency and ecological validity of personality structure in common marmosets (Callithrix jacchus): a unifying field and laboratory approach. Am. J. Primatol. 83, e23229. (10.1002/ajp.23229) PubMed DOI PMC
Šlipogor V, Burkart JM, Martin JS, Bugnyar T, Koski SE. 2020. Personality method validation in common marmosets (Callithrix jacchus): getting the best of both worlds. J. Comp. Psychol. 134, 52-70. (10.1037/com0000188) PubMed DOI
Masilkova M, Weiss A, Konečná M. 2018. How long does it take? Reliable personality assessment based on common behaviour in cotton-top tamarins (Saguinus oedipus). Behav. Process. 157, 59-67. (10.1016/j.beproc.2018.08.009) PubMed DOI
Martin P, Bateson P. 2007. Measuring behaviour: an introductory guide, 3rd edn. Cambridge, UK: Cambridge University Press.
Shannon CE, Weaver W. 1963. The mathematical theory of communication. Urbana, IL: University of Illinois Press.
R Core Team 2020. R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. https://www.R-project.org/.
Gamer M, Lemon J, Fellows I, Singh P. 2019. Various Coefficients of Interrater Reliability and Agreement. R Package version 0.84.1.
Nakagawa S, Schielzeth H. 2010. Repeatability for Gaussian and non-Gaussian data: a practical guide for biologists. Biol. Rev. 85, 935-956. (10.1111/j.1469-185X.2010.00141.x) PubMed DOI
Stoffel M, Nakagawa S, Schielzeth H. 2019. rptR: repeatability estimation for Gaussian and Non-Gaussian Data. R Package version 0.9.22.
Revelle W. 2021. Procedures for Psychological, Psychometric and Personality Research. R Package version 2.2.5.
Horn JL. 1965. A rationale and test for the number of factors in factor analysis. Psychometrika 30, 179-185. (10.1007/BF02289447) PubMed DOI
Morton FB, Altschul D. 2019. Data reduction analyses of animal behaviour: avoiding Kaiser's criterion and adopting more robust automated methods. Anim. Behav. 149, 89-95. (10.1016/j.anbehav.2019.01.003) DOI
Dinno A. 2018. paran: Horn's test of principal components/factors. R Package version 1.5.2.
Wilson VAD, Inoue-Murayama M, Weiss A. 2018. A comparison of personality in the common and bolivian squirrel monkey (Saimiri sciureus and Saimiri boliviensis). J. Comp. Psychol. 132, 24-39. (10.1037/com0000093) PubMed DOI
Manson JH, Perry S. 2013. Personality structure, sex differences, and temporal change and stability in wild white-faced capuchins, Cebus capucinus. J. Comp. Psychol. 127, 299-311. (10.1037/a0031316) PubMed DOI
Gorsuch RL. 1983. Factor analysis, 2nd edn. Hillsdale, NJ: Lawrence Erlbaum Associates.
Budaev S V. 2010. Using principal components and factor analysis in animal behaviour research: caveats and guidelines. Ethology 116, 472-480. (10.1111/j.1439-0310.2010.01758.x) DOI
Kaiser HF. 1974. An index of factorial simplicity. Psychometrika 39, 31-36. (10.1007/BF02291575) DOI
Bartlett MS. 1954. A note on the multiplying factors for various χ2 approximations. J. R. Stat. Soc. Ser. B 16, 296-298. (10.1111/j.2517-6161.1954.tb00174.x) DOI
Koski SE, Buchanan-Smith HM, Burkart JM, Bugnyar T, Weiss A. 2017. Common marmoset (Callithrix jacchus) personality. J. Comp. Psychol. 131, 326-336. (10.1037/com0000089) PubMed DOI
Inoue-Murayama M, Yokoyama C, Yamanashi Y, Weiss A. 2018. Common marmoset (Callithrix jacchus) personality, subjective well-being, hair cortisol level and AVPR1a, OPRM1, and DAT genotypes. Sci. Rep. 8, 10255. (10.1038/s41598-018-28112-7) PubMed DOI PMC
Epple G. 1970. Quantitative studies on scent marking in the marmoset (Callithrix jacchus). Folia Primatol. 13, 48-62. (10.1159/000155308) PubMed DOI
Barros M, Boere V, Huston JP, Tomaz C. 2000. Measuring fear and anxiety in the marmoset (Callithrix penicillata) with a novel predator confrontation model: effects of diazepam. Behav. Brain Res. 108, 205-211. (10.1016/S0166-4328(99)00153-9) PubMed DOI
Kaplan G, Pines MK, Rogers LJ. 2012. Stress and stress reduction in common marmosets. Appl. Anim. Behav. Sci. 137, 175-182. (10.1016/j.applanim.2011.04.011) DOI
King JE, Weiss A, Sisco MM. 2008. Aping humans: age and sex effects in chimpanzee (Pan troglodytes) and human (Homo sapiens) personality. J. Comp. Psychol. 122, 418-427. (10.1037/a0013125) PubMed DOI
Chopik WJ, Kitayama S. 2018. Personality change across the life span: insights from a cross-cultural, longitudinal study. J. Pers. 86, 508-521. (10.1111/JOPY.12332) PubMed DOI PMC
Donnellan MB, Lucas RE. 2008. Age differences in the big five across the life span: evidence from two national samples. Psychol. Aging 23, 558-566. (10.1037/a0012897) PubMed DOI PMC
Kuhar CW, Stoinski TS, Lukas KE, Maple TL. 2006. Gorilla behavior index revisited: age, housing and behavior. Appl. Anim. Behav. Sci. 96, 315-326. (10.1016/j.applanim.2005.06.004) DOI
Seyfarth RM, Silk JB, Cheney DL. 2012. Variation in personality and fitness in wild female baboons. PNAS 109, 16 980-16 985. (10.1073/pnas.1210780109) PubMed DOI PMC
Silk JB, Beehner JC, Bergman TJ, Crockford C, Engh AL, Moscovice LR, Wittig RM, Seyfarth RM, Cheney DL. 2010. Strong and consistent social bonds enhance the longevity of female baboons. Curr. Biol. 20, 1359-1361. (10.1016/j.cub.2010.05.067) PubMed DOI
Weiss A, King JE. 2015. Great ape origins of personality maturation and sex differences: a study of orangutans and chimpanzees. J. Pers. Soc. Psychol. 108, 648-664. (10.1037/pspp0000022) PubMed DOI
Harrison LM, Noble DWA, Jennions MD. 2021. A meta-analysis of sex differences in animal personality: no evidence for the greater male variability hypothesis. Biol. Rev. 97, 679-707. (10.1111/brv.12818) PubMed DOI
Šlipogor V, Graf C, Massen JJM, Bugnyar T. 2022. Personality and social environment predict cognitive performance in common marmosets (Callithrix jacchus). Sci. Rep. 12, 6702. (10.1038/s41598-022-10296-8) PubMed DOI PMC
Hook MA, Rogers LJ. 2008. Visuospatial reaching preferences of common marmosets (Callithrix jacchus): an assessment of individual biases across a variety of tasks. J. Comp. Psychol. 122, 41-51. (10.1037/0735-7036.122.1.41) PubMed DOI
Díaz S, Murray L, Roberts SGB, Rodway P. 2021. Between-task consistency, temporal stability and the role of posture in simple reach and fishing hand preference in chimpanzees (Pan troglodytes). Appl. Anim. Behav. Sci. 242, 105417. (10.1016/j.applanim.2021.105417) DOI
Masilkova M, Šlipogor V, Lima Marques Silva GH, Hadová M, Lhota S, Bugnyar T, Konečná M. 2022. Age, but not hand preference, is related to personality traits in common marmosets (Callithrix jacchus). Figshare. (10.6084/m9.figshare.c.6249011) PubMed DOI PMC
figshare
10.6084/m9.figshare.c.6249011