International Journal of Primatology

, Volume 35, Issue 1, pp 288–304 | Cite as

Kinship and Dominance Rank Influence the Strength of Social Bonds in Female Geladas (Theropithecus gelada)

  • Elizabeth Tinsley Johnson
  • Noah Snyder-Mackler
  • Jacinta C. Beehner
  • Thore J. Bergman


In many primates, close social relationships are associated with lower stress, better health, and increased life span. However, individuals do not form bonds indiscriminately; rather, they focus on a few primary partners. This suggests that the identity of the partner may be as important as the bond itself. Although dominance and kinship have repeatedly emerged as salient predictors of female relationships, most of this research comes from species with multimale, multifemale groups and strict dominance hierarchies. Further, kinship was typically determined based on either behavior or on known mother–daughter relationships alone. To understand the generality of previous findings, we use behavioral and genetic sampling to examine whether dominance rank and/or genetic relatedness mediate female social bonds in geladas (Theropithecus gelada) living in the Simien Mountains National Park, Ethiopia. First, we found that, even though females in the same unit are closely related, female geladas still preferentially bond with the closest of these relatives. Second, females that were close kin formed the strongest bonds with females of similar rank to themselves. Finally, rank disparity predicted grooming rates but did not predict whether females were nearest neighbors. This suggests that, in contrast with data from other cercopithecines, spatial proximity among females may be less indicative of strong social bonds for geladas, a species that routinely exhibits a high degree of spatial overlap with extra-unit individuals. Together, these results highlight the importance of combining genetic data with detailed behavioral observations to help us understand how individuals choose and interact with social partners.


Composite sociality index Elo-rating Grooming Proximity Relatedness Theropithecus gelada 



We thank, first, the guest editors, Dr. Lauren Brent and Dr. Amanda Melin, for inviting us to participate in this timely special issue on primate behavior and genetics. Second, we thank the Ethiopian Wildlife Conservation Authority and the wardens and staff of the Simien Mountains National Park for granting us permission to conduct this research. We also could not have done this research without all the tireless data collection from all members of the University of Michigan Gelada Research Project across the years. Funding for this research was provided by the National Science Foundation (BCS-0715179, BCS-0824592, BCS-0962118), the Leakey Foundation, the National Geographic Society (Grant no. 8100-06), the University of Michigan, and the University of Pennsylvania. Drs. David Pappano and Eila Roberts gave thoughtful comments on an earlier draft of the manuscript. This research was approved by the University Committee on Use and Care of Animals (UCUCA no. 09554) at the University of Michigan and the University of Pennsylvania Institutional Animal Care and Use Committee (IACUC no. 802996), and adhered to the laws and guidelines of Ethiopia.

Supplementary material

10764_2013_9733_Fig4_ESM.jpg (71 kb)
Figure S1

(JPEG 71 kb)

10764_2013_9733_MOESM1_ESM.tiff (5.4 mb)
High resolution Image (TIFF 5541 kb)


  1. Albers, P. C., & de Vries, H. (2001). Elo-rating as a tool in the sequential estimation of dominance strengths. Animal Behaviour, 61, 489–495.CrossRefGoogle Scholar
  2. Altmann, J. (1974). Observational study of behavior: Sampling methods. Behaviour, 49, 227–267.PubMedCrossRefGoogle Scholar
  3. Barrett, L., & Henzi, S. P. (2002). Constraints on relationship formation among female primates. Behaviour, 139, 263–289.CrossRefGoogle Scholar
  4. Bergman, T. J. (2010). Experimental evidence for limited vocal recognition in a wild primate: Implications for the social complexity hypothesis. Proceedings of the Royal Society B: Biological Sciences, 277, 3045–3053.PubMedCrossRefGoogle Scholar
  5. Bernstein, I. S., & Ehardt, C. L. (1985). Agonistic aiding: Kinship, rank, age, and sex influences. American Journal of Primatology, 8, 37–52.CrossRefGoogle Scholar
  6. Brent, L. J., Semple, S., Dubuc, C., Heistermann, M., & Maclarnon, A. (2011). Social capital and physiological stress levels in free-ranging adult female rhesus macaques. Physiology & Behavior, 102, 76–83.CrossRefGoogle Scholar
  7. Chapais, B., & Berman, C. M. (Eds.). (2004). Kinship and behavior in primates. Oxford: Oxford University Press.Google Scholar
  8. Chapais, B., Gauthier, C., Prudhomme, J., & Vasey, P. (1997). Relatedness threshold for nepotism in Japanese macaques. Animal Behaviour, 53, 1089–1101.CrossRefGoogle Scholar
  9. Chapais, B., Savard, L., & Gauthier, C. (2001). Kin selection and the distribution of altruism in relation to degree of kinship in Japanese macaques (Macaca fuscata). Behavioral Ecology and Sociobiology, 49, 493–502.CrossRefGoogle Scholar
  10. Charpentier, M., Deubel, D., & Peignot, P. (2008). Relatedness and social behavior in Cercopithecus solatus. International Journal of Primatology, 29, 487–495.CrossRefGoogle Scholar
  11. Cords, M. (2012). The behavior, ecology and social evolution of Cercopithecine monkeys. In J. Mitani, J. Call, P. Kappeler, R. Palombit, & J. Silk (Eds.), The evolution of primate societies (pp. 91–112). Chicago: University of Chicago Press.Google Scholar
  12. Crockford, C., Wittig, R. M., Whitten, P. L., Seyfarth, R. M., & Cheney, D. L. (2008). Social stressors and coping mechanisms in wild female baboons (Papio hamadryas ursinus). Hormones and Behavior, 53, 254–265.PubMedCrossRefGoogle Scholar
  13. Csillëry, K., Johnson, T., Beraldi, D., Clutton-Brock, T., Coltman, D., Hansson, B., et al. (2006). Performance of marker-based relatedness estimators in natural populations of outbred vertebrates. Genetics, 173, 2091–2101.PubMedCrossRefGoogle Scholar
  14. de Waal, F. B. M. (1991). Rank distance as a central feature of rhesus monkey social organization: A sociometric analysis. Animal Behaviour, 41, 383–395.CrossRefGoogle Scholar
  15. Dunbar, R. I. M. (1977). Feeding ecology of gelada baboons: A preliminary report. In T. H. Clutton-Brock (Ed.), Primate ecology (pp. 20–273). London: Academic Press.Google Scholar
  16. Dunbar, R. I. M. (1979). Structure of gelada baboon reproductive units: I. Stability of social relationships. Behaviour, 69, 72–87.CrossRefGoogle Scholar
  17. Dunbar, R. I. M. (1984). Reproductive decisions: An economic analysis of gelada baboon social strategies. Princeton, NJ: Princeton University Press.Google Scholar
  18. Dunbar, R. I. M. (1992). A model of the gelada socioecological system. Primates, 33, 69–83.CrossRefGoogle Scholar
  19. Dunbar, R. I. M. (1996). Grooming, gossip, and the evolution of language. Cambridge, MA: Harvard University Press.Google Scholar
  20. Dunbar, R. I. M., & Bose, U. (1991). Adaptation to grass-eating in gelada baboons. Primates, 32, 1–7.CrossRefGoogle Scholar
  21. Dunbar, R. I. M., & Dunbar, P. (1988). Maternal time budgets of gelada baboons. Animal Behaviour, 36, 970–980.CrossRefGoogle Scholar
  22. Dunbar, R. I. M., & Shultz, S. (2010). Bondedness and sociality. Behaviour, 147, 775–803.CrossRefGoogle Scholar
  23. Elo, A. E. (1961). New USCF rating system. Chess Life, 16, 160–161.Google Scholar
  24. Elo, A. E. (1978). The rating of chessplayers, past and present. London: Batsford.Google Scholar
  25. Engh, A. L., Beehner, J. C., Bergman, T. J., Whitten, P. L., Hoffmeier, R. R., Seyfarth, R. M., et al. (2006). Behavioural and hormonal responses to predation in female chacma baboons (Papio hamadryas ursinus). Proceedings of the Royal Society B: Biological Sciences, 273, 707–712.PubMedCrossRefGoogle Scholar
  26. Fashing, P. J., Nguyen, N., & Fashing, N. J. (2010). Behavior of geladas and other endemic wildlife during a desert locus outbreak at Guassa, Ethiopia: Ecological and conservation implications. Primates, 51, 193–197.PubMedCrossRefGoogle Scholar
  27. Fedigan, L. (1993). Sex differences and intersexual relations in adult white-faced capuchins (Cebus capucinus). International Journal of Primatology, 14, 853–877.CrossRefGoogle Scholar
  28. Hamilton, W. D. (1964). The genetical evolution of social behavior: I and II. Journal of Theoretical Biology, 7, 1–52.PubMedCrossRefGoogle Scholar
  29. Iwamoto, T. (1979). Feeding ecology. In M. Kawai (Ed.), Ecological and sociological studies of gelada baboons (pp. 279–330). Tokyo: Kodansha.Google Scholar
  30. Jack, K. M., & Fedigan, L. M. (2004). Male dispersal patterns in white-faced capuchins, Cebus capucinus. Part 1: Patterns and causes of natal emigration. Animal Behaviour, 67, 761–769.CrossRefGoogle Scholar
  31. Kapsalis, E. (2004). Matrilineal kinship and primate behavior. In B. Chapais & C.M. Berman (Ed.), Kinship and behavior in primates (pp. 153–176). Oxford: Oxford University Press.Google Scholar
  32. King, A. J., Clark, F. E., & Cowlishaw, G. (2011). The dining etiquette of desert baboons: The roles of social bonds, kinship, and dominance in co-feeding networks. American Journal of Primatology, 73, 768–774.PubMedCrossRefGoogle Scholar
  33. Langergraber, K., Mitani, J., & Vigilant, L. (2009). Kinship and social bonds in female chimpanzees (Pan troglodytes). American Journal of Primatology, 71, 840–851.PubMedCrossRefGoogle Scholar
  34. le Roux, A., Beehner, J. C., & Bergman, T. J. (2011). Female philopatry and dominance patterns in wild geladas. American Journal of Primatology, 73, 422–430.PubMedCrossRefGoogle Scholar
  35. Mitani, J. C. (2009). Male chimpanzees form enduring and equitable social bonds. Animal Behaviour, 77, 633–640.CrossRefGoogle Scholar
  36. Mitani, J. C., Call, J., Kappeler, P. M., Palombit, R. A., & Silk, J. B. (Eds.). (2012). The evolution of primate societies. Chicago: The University of Chicago Press.Google Scholar
  37. Nakamichi, M., & Shizawa, Y. (2003). Distribution of grooming among adult females in a large, free-ranging group of Japanese macaques. International Journal of Primatology, 24, 607–625.CrossRefGoogle Scholar
  38. Neumann, C., Duboscq, J., Dubuc, C., Ginting, A., Irwan, A. M., Agil, M., et al. (2011). Assessing dominance hierarchies: Validation and advantages of progressive evaluation with Elo-rating. Animal Behaviour, 82, 911–921.CrossRefGoogle Scholar
  39. Perry, S. (1996). Female-female social relationships in wild white-faced capuchin monkeys, Cebus capucinus. American Journal of Primatology, 40, 167–182.CrossRefGoogle Scholar
  40. Perry, S., Manson, J. H., Muniz, L., Gros-Luis, J., & Vigilant, L. (2008). Kin-biased social behaviour in wild female white-faced capuchins, Cebus capucinus. Animal Behaviour, 76, 187–199.CrossRefGoogle Scholar
  41. R Development Core Team. (2013). R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.Google Scholar
  42. Range, F., & Noë, R. (2002). Familiarity and dominance relations among female sooty mangabeys in the Taï National Park. American Journal of Primatology, 56, 137–153.PubMedCrossRefGoogle Scholar
  43. Sarkar, D., & Bates, D. (2009). lme4: Linear mixed-effects models using S4 classes. R package version 0.999999–2. Available at:
  44. Schino, G. (2001). Grooming, competition and social rank among female primates: A meta-analysis. Animal Behaviour, 62, 265–271.CrossRefGoogle Scholar
  45. Schülke, O., Bhagavatula, J., Vigilant, L., & Ostner, J. (2010). Social bonds enhance reproductive success in male macaques. Current Biology, 20, 2207–2210.PubMedCrossRefGoogle Scholar
  46. Schülke, O., Wenzel, S., & Ostner, J. (2013). Paternal relatedness predicts the strength of social bonds among female rhesus macaques. PLoS ONE, 8, e59789.PubMedCentralPubMedCrossRefGoogle Scholar
  47. Seyfarth, R. M. (1976). Social relationships among adult female baboons. Animal Behaviour, 24, 917–938.CrossRefGoogle Scholar
  48. Seyfarth, R. M. (1977). A model of social grooming among adult female monkeys. Journal of Theoretical Biology, 65, 671–698.PubMedCrossRefGoogle Scholar
  49. Silk, J. B. (1982). Altruism among female Macaca radiata – explanations and analysis of patterns of grooming and coalition formation. Behaviour, 79, 162–188.CrossRefGoogle Scholar
  50. Silk, J. B. (2002). Kin selection in primate groups. International Journal of Primatology, 23, 849–875.CrossRefGoogle Scholar
  51. Silk, J. B., Seyfarth, R. M., & Cheney, D. L. (1999). The structure of social relationships among female savanna baboons in Moremi Reserve, Botswana. Behaviour, 136, 679–703.CrossRefGoogle Scholar
  52. Silk, J. B., Alberts, S. C., & Altmann, J. (2006a). Social relationships among adult female baboons (Papio cynocephalus): II. Variation in the quality and stability of social bonds. Behavioral Ecology and Sociobiology, 61, 197–204.CrossRefGoogle Scholar
  53. Silk, J. B., Altmann, J., & Alberts, S. C. (2006b). Social relationships among adult female baboons (Papio cynocephalus): I. Variation in the strength of social bonds. Behavioral Ecology and Sociobiology, 61, 183–195.CrossRefGoogle Scholar
  54. Silk, J. B., Beehner, J. C., Bergman, T. J., Crockford, C., Engh, A. L., Moscovice, et al. (2009). The benefits of social capital: Close social bonds among female baboons enhance offspring survival. Proceedings of the Royal Society B: Biological Sciences, 276, 3099–3104.PubMedCrossRefGoogle Scholar
  55. Silk, J. B., Beehner, J. C., Bergman, T. J., Crockford, C., Engh, A. L., Moscovice, L. R., et al. (2010). Female chacma baboons form strong, equitable, and enduring social bonds. Behavioral Ecology and Sociobiology, 64, 1733–1747.PubMedCentralPubMedCrossRefGoogle Scholar
  56. Silk, J. B., Alberts, S. C., Altmann, J., Cheney, D. L., & Seyfarth, R. M. (2012). Stability of partner choice among female baboons. Animal Behaviour, 83, 1511–1518.PubMedCentralPubMedCrossRefGoogle Scholar
  57. Smith, K., Alberts, S. C., & Altmann, J. (2003). Wild female baboons bias their social behaviour towards paternal half-sisters. Proceedings of the Royal Society B: Biological Sciences, 270, 503–510.PubMedCrossRefGoogle Scholar
  58. Snyder-Mackler, N., Alberts, S. C., & Bergman, T. J. (2012a). Concessions of an alpha male? Cooperative defence and shared reproduction in multi-male primate groups. Proceedings of the Royal Society B: Biological Sciences, 279, 3788–3795.PubMedCrossRefGoogle Scholar
  59. Snyder-Mackler, N., Beehner, J. C., & Bergman, T. J. (2012b). Defining higher levels in the multilevel societies of geladas (Theropithecus gelada). International Journal of Primatology, 33, 1054–1068.CrossRefGoogle Scholar
  60. Sterck, E. H., Watts, D. P., & van Schaik, C. P. (1997). The evolution of female social relationships in nonhuman primates. Behavioral Ecology and Sociobiology, 41, 291–309.CrossRefGoogle Scholar
  61. Van Horn, R. C., Altmann, J., & Alberts, S. C. (2008). Can’t get there from here: Inferring kinship from pairwise genetic relatedness. Animal Behaviour, 75, 1173–1180.CrossRefGoogle Scholar
  62. van Schaik, C. P. (1989). The ecology of social relationships amongst female primates. In V. Standen & R. A. Foley (Eds.), Comparative socioecology: The behavioural ecology of humans and other mammals (pp. 195–218). Oxford: Blackwell.Google Scholar
  63. Wang, J. (2002). An estimator for pairwise relatedness using molecular markers. Genetics, 160, 1203–1215.PubMedGoogle Scholar
  64. Widdig, A., Nürnberg, P., Krawczak, M., Streich, W. J., & Bercovitch, F. (2002). Affiliation and aggression among adult female rhesus macaques: A genetic analysis of paternal cohorts. Behaviour, 139, 371–391.CrossRefGoogle Scholar
  65. Wrangham, R. W. (1980). An ecological model of female-bonded primate groups. Behaviour, 75, 262–300.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  • Elizabeth Tinsley Johnson
    • 1
  • Noah Snyder-Mackler
    • 2
  • Jacinta C. Beehner
    • 3
  • Thore J. Bergman
    • 4
  1. 1.Department of AnthropologyUniversity of MichiganAnn ArborUSA
  2. 2.Department of Evolutionary AnthropologyDuke UniversityDurhamUSA
  3. 3.Departments of Anthropology and PsychologyUniversity of MichiganAnn ArborUSA
  4. 4.Departments of Psychology and Ecology & Evolutionary BiologyUniversity of MichiganAnn ArborUSA

Personalised recommendations