Advertisement

International Journal of Primatology

, Volume 35, Issue 1, pp 188–209 | Cite as

Personality Traits in Rhesus Macaques (Macaca mulatta) Are Heritable but Do Not Predict Reproductive Output

  • Lauren J. N. BrentEmail author
  • Stuart Semple
  • Ann MacLarnon
  • Angelina Ruiz-Lambides
  • Janis Gonzalez-Martinez
  • Michael L. Platt
Article

Abstract

There is growing evidence that behavioral tendencies, or “personalities,” in animals are an important aspect of their biology, yet their evolutionary basis is poorly understood. Specifically, how individual variation in personality arises and is subsequently maintained by selection remains unclear. To address this gap, studies of personality require explicit incorporation of genetic information. Here, we explored the genetic basis of personality in rhesus macaques by determining the heritability of personality components and by examining the fitness consequences of those components. We collected observational data for 108 adult females living in three social groups in a free-ranging population via focal animal sampling. We applied principal component analysis to nine spontaneously occurring behaviors and identified six putative personality components, which we named Meek, Bold, Aggressive, Passive, Loner, and Nervous. All components were repeatable and heritable, with heritability estimates ranging from 0.14 to 0.35. We found no evidence of an association with reproductive output, measured either by infant survival or by interbirth interval, for any of the personality components. This finding suggests either that personality does not have fitness-related consequences in this population or that selection has acted to reduce fitness-associated variation in personality.

Keywords

Additive genetic variance Behavioral tendencies Fitness Quantitative genetics Reproductive success 

Notes

Acknowledgments

We thank Bonn Aure, Jacqueline Buhl, Monica Carlson, Sam Larson, Elizabeth Maldonado, Heather Sherwin, and the Cayo Santiago Staff for research support. We thank Greg Blomquist and John Pearson for statistical advice and assistance, and Amanda Melin and two anonymous reviewers for helpful comments on the manuscript. The authors were supported by NIMH grants R01-MH089484 and R01-MH096875, an Incubator Award from the Duke Institute for Brain Sciences. L. J. N. Brent was supported by fellowships from the Natural Sciences and Engineering Research Council of Canada (NSERC), the University of Roehampton, and the Duke Center for Interdisciplinary Decision Sciences. The CPRC is supported by grant 8-P40 OD012217-25 from the National Center for Research Resources (NCRR) and the Office of Research Infrastructure Programs (ORIP) of the National Institutes of Health.

References

  1. Adams, M. J., King, J. E., & Weiss, A. (2012). The majority of genetic variation in orangutan personality and subjective well-being is nonadditive. Behavior Genetics, 42, 675–686.PubMedCrossRefGoogle Scholar
  2. Almasy, L., & Blangero, J. (1998). Multipoint quantitative-trait linkage analysis. American Journal of Human Genetics, 62, 1198–1211.PubMedCentralPubMedCrossRefGoogle Scholar
  3. Arnold, S., Pfrender, M., & Jones, A. (2001). The adaptive landscape as a conceptual bridge between micro- and macroevolution. Genetica, 112–113, 9–32.PubMedCrossRefGoogle Scholar
  4. Bakker, T. C. M. (1986). Aggressiveness in sticklebacks (Gasterosteus aculeatus L.): a behaviour-genetic study. Behaviour, 98, 1–144.CrossRefGoogle Scholar
  5. Bize, P., Diaz, C., & Lindström, J. (2012). Experimental evidence that adult antipredator behaviour is heritable and not influenced by behavioural copying in a wild bird. Proceedings of the Royal Society B: Biological Sciences, 279, 1380–1388.PubMedCrossRefGoogle Scholar
  6. Blomquist, G. E. (2009). Fitness-related patterns of genetic variation in rhesus macaques. Genetica, 135, 209–219.PubMedCrossRefGoogle Scholar
  7. Blomquist, G. E., & Brent, L. J. N. (2013). Applying quantitative genetic methods to primate social behavior. International Journal of Primatology. doi: 10.1007/s10764-013-9709-5.
  8. Bouchard, T. J., Jr., & Loehlin, J. C. (2001). Genes, evolution, and personality. Behavior Genetics, 31(3), 243–273.PubMedCrossRefGoogle Scholar
  9. Brent, L. J. N. (2010). Investigating the causes and consequences of sociality in adult female rhesus macaques using a social network approach. PhD Thesis, University of Roehampton.Google Scholar
  10. Brent, L. J. N., Heilbronner, S. R., Horvath, J. E., Gonzalez-Martinez, J., Ruiz-Lambides, A., Robinson, A. G., et al. (2013a). Genetic origins of social networks in rhesus macaques. Scientific Reports. doi: 10.1038/srep01042.PubMedCentralPubMedGoogle Scholar
  11. Brent, L. J. N., MacLarnon, A., Platt, M. L., & Semple, S. (2013b). Seasonal changes in the structure of rhesus macaque social networks. Behavioral Ecology and Sociobiology, 67, 349–359.PubMedCrossRefGoogle Scholar
  12. Capitanio, J. P. (1999). Personality dimensions in adult male rhesus macaques: prediction of behaviors across time and situation. American Journal of Primatology, 47, 299–320.PubMedCrossRefGoogle Scholar
  13. Charmantier, A., Buoro, M., Gimenez, O., & Weimerskirch, H. (2011). Heritability of short-scale natal dispersal in a large-scale foraging bird, the wandering albatross. Journal of Evolutionary Biology, 24, 1487–1496.PubMedCrossRefGoogle Scholar
  14. Chikazawa, D., Gordon, T. P., Bean, C. A., & Bernstein, I. S. (1979). Mother-daughter dominance reversals in rhesus monkeys (Macaca mulatta). Primates, 20, 301–305.CrossRefGoogle Scholar
  15. Cloninger, C. R., Przybeck, T. R., & Svrakic, D. M. (1991). The tridimensional personality questionnaire: United States normative data. Psychological Reports, 69, 1047–1057.PubMedCrossRefGoogle Scholar
  16. Cords, M. (2012). The behavior, ecology and social evolution of Cercopithecine monkeys. In J. C. Mitani, J. Call, P. M. Kappeler, R. A. Palombit, & J. B. Silk (Eds.), The evolution of primate societies (pp. 91–112). Chicago: University of Chicago Press.Google Scholar
  17. Datta, S. (1988). The acquisition of dominance among free-ranging rhesus monkey siblings. Animal Behaviour, 36, 754–772.CrossRefGoogle Scholar
  18. Dingemanse, N. J., Both, C., Drent, P. J., Van Oers, K., & Van Noordwijk, A. J. (2002). Repeatability and heritability of exploratory behaviour in great tits from the wild. Animal Behaviour, 64, 929–938.CrossRefGoogle Scholar
  19. Dingemanse, N. J., Both, C., Drent, P. J., & Tinbergen, J. M. (2004). Fitness consequences of avian personalities in a fluctuating environment. Proceedings of the Royal Society of London B: Biological Sciences, 271, 847–852.CrossRefGoogle Scholar
  20. Dochtermann, N. A., & Roff, D. A. (2010). Applying a quantitative genetics framework to behavioural syndrome research. Philosophical Transactions of the Royal Society B: Biological Sciences, 365, 4013–4020.CrossRefGoogle Scholar
  21. Elston, D. A., Moss, R., Boulinier, T., Arrowsmith, C., & Lambin, X. (2001). Analysis of aggregation, a worked example: numbers of ticks on red grouse chicks. Parasitology, 122, 563–569.PubMedCrossRefGoogle Scholar
  22. Endler, J. A. (1986). Natural selection in the wild. Princeton: Princeton University Press.Google Scholar
  23. Fairbanks, L. A., Newman, T. K., Bailey, J. N., Jorgensen, M. J., Breidenthal, S. E., Ophoff, R. A., et al. (2004). Genetic contributions to social impulsivity and aggressiveness in vervet monkeys. Biological Psychiatry, 55(6), 642–647.PubMedCrossRefGoogle Scholar
  24. Falconer, D. S., & Mackay, T. F. C. (1996). Introduction to quantitative genetics. New York: Longman.Google Scholar
  25. Feil, R., & Fraga, M. F. (2012). Epigenetics and the environment: emerging patterns and implications. Nature Reviews Genetics, 13, 97–109.PubMedGoogle Scholar
  26. Fisher, R. A. (1930). The genetical theory of natural selection. Oxford: Clarendon Press.Google Scholar
  27. Gosling, S. D., Lilienfeld, S. O., & Marino, L. (2003). Personality. In D. Maestripieri (Ed.), Primate psychology (pp. 254–288). Cambridge: Harvard University Press.Google Scholar
  28. Hadfield, J. (2010). MCMC methods for multi-response generalised linear mixed models: the MCMCglmm R package. Journal of Statistical Software, 33, 1–22.Google Scholar
  29. Hadidian, J., & Bernstein, I. S. (1979). Female reproductive cycles and birth data from an Old World monkey colony. Primates, 20, 429–442.CrossRefGoogle Scholar
  30. Johnson, A. M., Vernon, P. A., & Feiler, A. R. (2008). Behavioral genetic studies of personality: An introduction and review of the results of 50+ years of research. In G. Boyle, G. Matthews, & D. Saklofske (Eds.), Handbook of personality theory and assessment (pp. 145–173). London: SAGE.Google Scholar
  31. Konečná, M., Lhota, S., Weiss, A., Urbánek, T., Adamová, T., & Pluháček, J. (2008). Personality in free-ranging Hanuman langur (Semnopithecus entellus) males: subjective ratings and recorded behavior. Journal of Comparative Psychology, 122, 379–389.PubMedCrossRefGoogle Scholar
  32. Kralj-Fiser, S., Weiss, B. M., & Kotrschal, K. (2010). Behavioural and physiological correlates of personality in greylag geese (Anser anser). Journal of Ethology, 28, 363–370.CrossRefGoogle Scholar
  33. Krause, J., James, R., & Croft, D. P. (2010). Personality in the context of social networks. Philosophical Transactions of the Royal Society B: Biological Sciences, 365, 4099–4106.CrossRefGoogle Scholar
  34. Lande, R. (1979). Quantitative genetic analysis of multivariate evolution, applied to brain: body size allometry. Evolution, 402–416.Google Scholar
  35. Lande, R., & Arnold, S. J. (1983). The measurement of selection on correlated characters. Evolution, 37(6), 1210–1226.CrossRefGoogle Scholar
  36. Lynch, M., & Walsh, B. (1998). Genetics and analysis of quantitative traits. Sunderland: Sinauer Associates.Google Scholar
  37. Majolo, B., Lehmann, J., Vizioli, A. D., & Schino, G. (2012). Fitness-related benefits of dominance in primates. American Journal of Physical Anthropology, 147, 652–660.PubMedCrossRefGoogle Scholar
  38. McCrae, R. R., & Costa, P. T. (1999). A five-factor theory of personality. In L. A. Pervin & O. P. John (Eds.), Handbook of personality: Theory and research (2nd ed., pp. 139–153). New York: Guilford Press.Google Scholar
  39. Morrissey, M., Kruuk, L., & Wilson, A. (2010). The danger of applying the breeder's equation in observational studies of natural populations. Journal of Evolutionary Biology, 23, 2277–2288.PubMedCrossRefGoogle Scholar
  40. Nakagawa, S., & Schielzeth, H. (2010). Repeatability for Gaussian and non-Gaussian data: a practical guide for biologists. Biological Reviews of the Cambridge Philosophical Society, 85, 935–956.PubMedGoogle Scholar
  41. Pilia, G., Chen, W.-M., Scuteri, A., Orrú, M., Albai, G., Dei, M., et al. (2006). Heritability of cardiovascular and personality traits in 6,148 Sardinians. PLoS Genetics, 2, e132.Google Scholar
  42. Price, T., Kirkpatrick, M., & Arnold, S. (1988). Directional selection and the evolution of breeding date in birds. Science, 240, 798–799.PubMedCrossRefGoogle Scholar
  43. Rawlings, R. G., & Kessler, M. J. (Eds.). (1986). The Cayo Santiago macaques. Albany: State University of New York Press.Google Scholar
  44. Reale, D., & Festa-Bianchet, M. (2003). Predator-induced natural selection on temperament in bighorn ewes. Animal Behaviour, 65, 463–470.CrossRefGoogle Scholar
  45. Robertson, A. (1966). A mathematical model of the culling process in dairy cattle. Animal Production, 8, 108.Google Scholar
  46. Rogers, J., Shelton, S. E., Shelledy, W., Garcia, R., & Kalin, N. H. (2008). Genetic influences on behavioral inhibition and anxiety in juvenile rhesus macaques. Genes, Brain and Behavior, 7, 463–469.CrossRefGoogle Scholar
  47. Schino, G., Perretta, G., Taglioni, A. M., Monaco, V., & Troisi, A. (1996). Primate displacement activities as an ethopharmacological model of anxiety. Anxiety, 2, 186–191.PubMedCrossRefGoogle Scholar
  48. Seyfarth, R. M., Silk, J. B., & Cheney, D. L. (2012). Variation in personality and fitness in wild female baboons. Proceedings of the National Academy of Sciences, 109, 16980–16985.CrossRefGoogle Scholar
  49. Sih, A., Bell, A. M., Johnson, J. C., & Ziemba, R. E. (2004). Behavioral syndromes: an integrative overview. Quarterly Review of Biology, 79, 241–277.PubMedCrossRefGoogle Scholar
  50. Sinn, D. L., Apiolaza, L. A., & Moltschaniwskyj, N. A. (2006). Heritability and fitness-related consequences of squid personality traits. Journal of Evolutionary Biology, 19, 1437–1447.PubMedCrossRefGoogle Scholar
  51. Smith, B. R., & Blumstein, D. T. (2008). Fitness consequences of personality: a meta-analysis. Behavioral Ecology, 19, 448–455.CrossRefGoogle Scholar
  52. Stevenson-Hinde, J., & Zunz, M. (1978). Subjective assessment of individual rhesus macaques. Primates, 19, 473–482.CrossRefGoogle Scholar
  53. Stinchcombe, J. R., Agrawal, A. F., Hohenlohe, P. A., Arnold, S. J., & Blows, M. W. (2008). Estimating nonlinear selection gradients using quadratic regression coefficients: double or nothing ? Evolution, 62, 2435–2440.PubMedCrossRefGoogle Scholar
  54. Suomi, S. J. (2006). Risk, resilience, and gene × environment interactions in rhesus monkeys. Annals of the New York Academy of Sciences, 1994, 52–62.CrossRefGoogle Scholar
  55. Taylor, R. W., Boon, A. K., Dantzer, B., Reale, D., Humphries, M. M., Boutin, S., Gorrell, J. C., Coltman, D. W., & McAdam, A. G. (2012). Low heritabilities, but genetic and maternal correlations between red squirrel behaviours. Journal of Evolutionary Biology, 25, 614–624.Google Scholar
  56. Thierry, B. (2004). Social epigenesis. In B. Thierry, M. Singh, & W. Kaumanns (Eds.), Macaque societies: A model for the study of social organization (pp. 267–290). Cambridge: Cambridge University Press.Google Scholar
  57. Uher, J., & Asendorpf, J. B. (2008). Personality assessment in the Great Apes: comparing ecologically valid behavior measures, behavior ratings, and adjective ratings. Journal of Research in Personality, 42, 821–838.CrossRefGoogle Scholar
  58. van Oers, K., & Mueller, J. C. (2010). Evolutionary genomics of animal personality. Philosophical Transactions of the Royal Society of London B: Biological Sciences, 365, 3991–4000.PubMedCrossRefGoogle Scholar
  59. van Oers, K., Drent, P. J., de Goede, P., & van Noordwijk, A. J. (2004). Realized heritability and repeatability of risk-taking behaviour in relation to avian personalities. Proceedings of the Royal Society of London B: Biological Sciences, 271, 65–73.CrossRefGoogle Scholar
  60. van Oers, K., de Jong, G., van Noordwijk, A. J., Kempenaers, B., & Drent, P. J. (2005). Contribution of genetics to the study of animal personalities: a review of case studies. Behaviour, 142, 1185–1206.CrossRefGoogle Scholar
  61. Visscher, P. M., Hill, W. G., & Wray, N. R. (2008). Heritability in the genomics era: concepts and misconceptions. Nature Reviews Genetics, 9, 255–266.PubMedCrossRefGoogle Scholar
  62. Weiss, A., King, J. E., & Figueredo, A. J. (2000). The heritability of personality factors in chimpanzees (Pan troglodytes). Behavior Genetics, 30, 213–221.PubMedCrossRefGoogle Scholar
  63. Weiss, A., King, J. E., & Enns, R. M. (2002). Subjective well-being is heritable and genetically correlated with dominance in chimpanzees (Pan troglodytes). Journal of Personality and Social Psychology, 83, 1141–1149.PubMedCrossRefGoogle Scholar
  64. Wilk, M. B., & Gnanadesikan, R. (1968). Probability plotting methods for the analysis for the analysis of data. Biometrika, 55, 1–17.PubMedGoogle Scholar
  65. Williamson, D. E., Coleman, K., Bacanu, S. A., Devlin, B. J., Rogers, J., Ryan, N. D., & Cameron, J. L. (2003). Heritability of fearful-anxious endophenotypes in infant rhesus macaques: a preliminary report. Biological Psychiatry, 53, 284–291.Google Scholar
  66. Wilson, A. J. (2008). Why h(2) does not always equal V-A/V-P? Journal of Evolutionary Biology, 21, 647–650.PubMedCrossRefGoogle Scholar
  67. Wilson, D. S., Clark, A. B., Coleman, K., & Dearstyne, T. (1994). Shyness and boldness in humans and other animals. Trends in Ecology & Evolution, 9, 442–446.CrossRefGoogle Scholar
  68. Wilson, A. J., Reale, D., Clements, M. N., Morrissey, M. M., Postma, E., Walling, C. A., et al. (2010). An ecologist's guide to the animal model. Journal of Animal Ecology, 79, 13–26.Google Scholar
  69. Wilson, A. D. M., Krause, S., Dingemanse, N. J., & Krause, J. (2013). Network position: a key component in the characterization of social personality types. Behavioral Ecology and Sociobiology, 67, 163–173.CrossRefGoogle Scholar
  70. Wolf, M., & Weissing, F. J. (2012). Animal personalities: consequences for ecology and evolution. Trends in Ecology & Evolution, 27, 452–461.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  • Lauren J. N. Brent
    • 1
    • 2
    Email author
  • Stuart Semple
    • 2
  • Ann MacLarnon
    • 2
  • Angelina Ruiz-Lambides
    • 3
  • Janis Gonzalez-Martinez
    • 3
  • Michael L. Platt
    • 1
    • 4
  1. 1.Duke Institute for Brain Sciences and Center for Cognitive NeuroscienceDuke UniversityDurhamUSA
  2. 2.Centre for Research in Evolutionary and Environmental AnthropologyUniversity of RoehamptonLondonUK
  3. 3.Caribbean Primate Research CenterUniversity of Puerto Rico, Medical Sciences CampusPunta SantiagoPuerto Rico
  4. 4.Departments of Neurobiology, Evolutionary Anthropology, and Psychology & NeuroscienceDuke UniversityDurhamUSA

Personalised recommendations