Skip to main content
SpringerLink
Log in

Variation in the Social Systems of Extant Hominoids: Comparative Insight into the Social Behavior of Early Hominins

  • Published:
International Journal of Primatology Aims and scope Submit manuscript

Abstract

The observed social systems of extant apes and humans suggest that the common ancestral state for Miocene hominoids was living in multimale–multifemale groups that exhibited a tendency to fission and fusion in response to ecological and/or social variables. The Hominoidea share a set of social commonalities, notably a social niche that extends beyond kin and beyond the immediate social group, as well as extensive intraspecific flexibility in social organization. We propose that an essential feature of hominoid evolution is the shift from limited plasticity in a generalized social ape to expanded behavioral plasticity as an adaptive niche. Whereas in most nonhominoid primates variability and flexibility take the shape of specific patterns of demographic flux and interindividual relationships, we can consider behavioral flexibility and plasticity as a means to an end in hominoid socioecological landscapes. In addition, the potential for innovation, spread, and inheritance of behavioral patterns and social traditions is much higher in the hominoids, especially the great apes, than in other anthropoid primates. We further suggest that this pattern forms a basis for the substantial expansion of social complexity and adaptive behavioral plasticity in the hominins, especially the genus Homo. Our objectives in this article are threefold: 1) summarize the variation in the social systems of extant hominoid taxa; 2) consider the evolutionary processes underlying these variations; and 3) expand upon the traditional socioecological model, especially with respect to reconstructions of early hominin social behavior. We emphasize a central role for both ecological and social niche construction, as well as behavioral plasticity, as basal hominoid characteristics. Over evolutionary time these characteristics influence the patterns of selection pressures and the resulting social structures. We propose that a mosaic of ecological and social inheritance patterns should be considered in the reconstruction of early hominin social systems.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Ahsan, F. (1995). Fighting between two females for a male in the Hoolock gibbon. International Journal of Primatology, 16, 731–737.

    Article  Google Scholar 

  • Alexander, R. D. (1989). Evolution of the human psyche. In P. Mellars & C. Stringer (Eds.), The human revolution: Behavioural and biological perspectives on the origins of modern humans (pp. 455–513). Princeton: Princeton University Press.

    Google Scholar 

  • Alexander, R. D. (1990). How did humans evolve? Reflections on the uniquely unique species. Museum of Zoology (Special Publication No. 1). Ann Arbor, MI: The University of Michigan Press.

  • Allman, J. M., Tetreault, N. A., Hakeem, A. Y., Manaye, K. F., Semendeferi, K., Erwin, J. M., Park, S., Goubert, V., & Hof, P. R. (2010). The von Economo neurons in the frontoinsular and anterior cingulate cortex in great apes and humans. Brain Structure & Function, 214, 495–517.

    Article  Google Scholar 

  • Arnason, U., Gullberg, A., Janke, A., & Xu, X. (1996). Pattern and timing of evolutionary divergences among hominoids based on analysis of complete mtDNAs. Journal of Molecular Evolution, 43, 650–661.

    Article  PubMed  CAS  Google Scholar 

  • Ashton, P. S. (1988). Dipterocarp biology as a window to the understanding of tropical forest structure. Annual Review of Ecological Systems, 19, 347–370.

    Article  Google Scholar 

  • Badrian, N. L., Badrian, A. J., & Susman, R. L. (1981). Preliminary observations on the feeding behaviour of Pan paniscus in the Lomako Forest of Central Zaire. Primates, 22, 173–181.

    Article  Google Scholar 

  • Badrian, N. L., & Malenky, R. K. (1984). Feeding ecology of Pan paniscus in the Lomako Forest, Zaire. In R. L. Susman (Ed.), The pygmy chimpanzee: Evolutionary biology and behaviour (pp. 275–299). New York: Plenum Press.

    Chapter  Google Scholar 

  • Bartlett, T. Q. (1999). The gibbons. In P. Dolhinow & A. Fuentes (Eds.), The nonhuman primates (pp. 44–49). Mountain View: Mayfield Publishing Company.

    Google Scholar 

  • Bartlett, T. Q. (2003). Intragroup and intergroup social interactions in white-handed gibbons. International Journal of Primatology, 24(2), 239–259.

    Article  Google Scholar 

  • Bartlett, T. Q. (2007). The hylobatidae: Small apes of asia. In C. J. Campbell, A. Fuentes, K. C. Mackinnon, M. Panger, & S. Bearder (Eds.), Primates in perspective (pp. 274–289). Oxford: Oxford University Press.

    Google Scholar 

  • Bartlett, T. Q. (2009). Seasonal home range use and defendability in white-handed gibbons (Hylobates lar) in Khao Yai National Park. In S. Lappan & D. J. Whittaker (Eds.), The gibbons: New perspectives on small ape socioecology and population biology (pp. 265–275). New York: Springer.

    Google Scholar 

  • Bleisch, W. V., & Chen, N. (1991). Ecology and behaviour of wild black-crested gibbons (Hylobates concolor) in China with a reconsideration of evidence for polygyny. Primates, 32, 539–548.

    Article  Google Scholar 

  • Boesch, C. (1994). Cooperative hunting in wild chimpanzees. Animal Behaviour, 48, 653–667.

    Article  Google Scholar 

  • Boesch, C., & Boesch-Achermann, H. (2000). The chimpanzees of the Tai Forest: Behavioural ecology and evolution. New York: Oxford University Press.

    Google Scholar 

  • Bradley, B. J., Doran-Sheehy, D. M., Lukas, D., Boesch, C., & Vigilant, L. (2004). Dispersed male networks in western gorillas. Current Biology, 14, 510–514.

    Article  PubMed  CAS  Google Scholar 

  • Brandon-Jones, D., Eudey, A. A., Geissmann, T., Groves, C. P., Melnick, D. J., Morales, J. C., Shekelle, M., & Stewart, C. B. (2004). Asian primate classification. International Journal of Primatology, 25, 97–164.

    Article  Google Scholar 

  • Brockelman, W. Y. (2009). Ecology and the social system of gibbons. In S. Lappan & D. J. Whittaker (Eds.), The gibbons: New perspectives on small ape socioecology and population biology (pp. 211–239). New York: Springer.

    Google Scholar 

  • Brockelman, W. Y., Reichard, U., Treesucon, U., & Raemaekers, J. J. (1998). Dispersal, pair formation and social structure in gibbons (Hylobates lar). Behavioural Ecology and Sociobiology, 42, 329–339.

    Article  Google Scholar 

  • Caldecott, J., & Ferriss, S. (2005). Gorilla overview. In J. Caldecott & L. Miles (Eds.), World atlas of great apes and their conservation (pp. 97–103). Berkeley: University of California Press.

    Google Scholar 

  • Chatterjee, H. J. (2006). Phylogeny and biogeography of gibbons: a dispersal-vicariance analysis. International Journal of Primatology, 27, 699–712.

    Article  Google Scholar 

  • Chatterjee, H. J. (2009). Evolutionary relationships among the gibbons: A biogeographic perspective. In S. Lappan & D. J. Whittaker (Eds.), The gibbons: New perspectives on small ape socioecology and population biology (pp. 13–36). New York: Springer.

    Google Scholar 

  • Chivers, D. J. (1974). The siamang in Malaya: a field study of a primate in tropical rain forest. Contributions to Primatology, 4, 1–335.

    PubMed  CAS  Google Scholar 

  • Choudhury, A. (1990). Population dynamics of Hoolock (Hylobates hoolock) in Assam, India. American Journal of Primatology, 20, 37–41.

    Article  Google Scholar 

  • Cipolletta, C. (2004). Effects of group dynamics and diet on the ranging patterns of a western gorilla group (Gorilla gorilla gorilla) at Bai Hokou, Central African Republic. American Journal of Primatology, 64, 193–206.

    Article  PubMed  Google Scholar 

  • Clutton-Brock, T. H. (1974). Primate social organization and ecology. Nature, 250, 539–542.

    Article  Google Scholar 

  • Clutton-Brock, T. H., & Harvey, P. H. (1977). Primate ecology and social organization. Journal of Zoology, 183(1), 1–39.

    Article  Google Scholar 

  • Conroy, G. C. (1990). Primate evolution. New York: W. W. Norton.

    Google Scholar 

  • Curran, L. M., Caniago, I., Paoli, G. D., Astiani, D., Kusneti, M., Leighton, M., Nirarita, C. E., & Haeruman, H. (1999). Impact of El Nino and logging on canopy tree recruitment in Borneo. Science, 286, 2184–2188.

    Article  PubMed  CAS  Google Scholar 

  • Das, J., & Biswas, J. (2009). Review of western hoolock gibbon (Hoolock hoolock) and eastern gibbon (Hoolock leuconedys) diversity with a presence of another new distinct variety of gibbon in Arunachal Pradesh, India. American Journal of Primatology, 71(Supplement 1), 72.

    Google Scholar 

  • Doran, D. M., Jungers, W. L., Sugiyama, Y., Fleagle, J. G., & Heesy, C. P. (2002). Multivariate and phylogenetic approaches to understanding chimpanzee and bonobo behavioural diversity. In C. Boesch, G. Hohmann, & L. Marchant (Eds.), Behavioural diversity in chimpanzees and bonobos (pp. 14–34). New York: Cambridge University Press.

    Chapter  Google Scholar 

  • Doran, D. M., & McNeilage, A. (1998). Gorilla ecology and behaviour. Evolutionary Anthropology, 6, 120–131.

    Article  Google Scholar 

  • Dunbar, R., Gamble, C., & Gowlett, J. (2010). Social brain, distributed mind. Proceedings of the British Academy, 158. New York, Oxford University Press.

  • Dunbar, R. I. M., & Shultz, S. (2007). Evolution in the social brain. Science, 317, 1344–1347.

    Article  PubMed  CAS  Google Scholar 

  • Easteal, S., & Herbert, G. (1997). Molecular evidence from the nuclear genome for the time frame of human evolution. Journal of Molecular Evolution, 44, S121–S132.

    Article  PubMed  CAS  Google Scholar 

  • Elder, A. A. (2009). Hylobatid diets revisited: The importance of body mass, fruit availability, and interspecific competition. In S. Lappan & D. J. Whittaker (Eds.), The gibbons: New perspectives on small ape socioecology and population biology (pp. 133–159). New York: Springer.

    Google Scholar 

  • Ellefson, J. O. (1974). Natural history of white-handed gibbons in the Malayan peninsula. Ph.D. dissertation, University of California, Berkeley.

  • Fan, P., Jiang, X., Liu, C., & Luo, W. (2006). Polygynous mating system and behavioural reason of black crested gibbon (Nomascus concolor jingdongensis) at Dazhaizi, Mt. Wuliang, Yunnan, China. Zoological Research, 27, 216–220.

    Google Scholar 

  • Flack, J. C., Girvan, M., de Waal, F. B. M., & Krakauer, D. C. (2006). Policing stabilizes construction of social niches in primates. Nature, 439, 426–429.

    Article  PubMed  CAS  Google Scholar 

  • Fleagle, J. G. (1999). Primate adaptation and evolution. San Diego: Academic.

    Google Scholar 

  • Fleming, T. H., Breitwisch, R., & Whitesides, G. H. (1987). Patterns of tropical vertebrate frugivore diversity. Annual Review of Ecological Systems, 18, 91–109.

    Article  Google Scholar 

  • Flinn, M. V., Geary, D. C., & Ward, C. V. (2005). Ecological dominance, social competition, and coalitionary arms races: why humans evolved extraordinary intelligence. Evolution and Human Behavior, 26, 10–46.

    Article  Google Scholar 

  • Foley, R., & Lee, P. C. (1989). Finite social space, evolutionary pathways, and reconstructing hominid evolution. Science, 243, 901–906.

    Article  PubMed  CAS  Google Scholar 

  • Fox, E. A., Sitompul, A. F., & van Schaik, C. P. (1999). Intelligent tool use in wild Sumatran orangutans. In S. T. Parker, R. W. Mitchell, & H. L. Miles (Eds.), The mentalities of gorillas and orangutans (pp. 99–116). Cambridge: Cambridge University Press.

    Chapter  Google Scholar 

  • Fox, E. A., van Schaik, C. P., Sitompul, A. F., & Doniele, N. W. (2004). Intra- and interpopulational differences in orangutan (Pongo pygmaeus) activity and diet: implications for the invention of tool use. American Journal of Physical Anthropology, 125, 162–174.

    Article  PubMed  Google Scholar 

  • Fuentes, A. (2000). Hylobatid communities: changing views on pair bonding and social organization in hominoids. Yearbook of Physical Anthropology, 43, 33–60.

    Article  Google Scholar 

  • Fuentes, A. (2002). Patterns and trends in primate pair bonds. International Journal of Primatology, 23, 953–978.

    Article  Google Scholar 

  • Fuentes, A. (2009). Evolution of human behaviour. New York: Oxford University Press.

    Google Scholar 

  • Fuentes, A. (2011). Social systems and socioecology: Understanding the evolution of primate behaviour. In C. Campbell, A. Fuentes, K. MacKinnon, S. Bearder, & R. Stumpf (Eds.), Primates in perspective (2nd ed., pp. 500–511). Oxford: Oxford University Press.

    Google Scholar 

  • Fuentes, A., Wyczalkowski, M., & MacKinnon, K. C. (2010). Niche construction through cooperation: a nonlinear dynamics contribution to modeling facets of the evolutionary history in the genus Homo. Current Anthropology, 51(3), 435–444.

    Article  Google Scholar 

  • Furuichi, T. (1987). Sexual swelling, receptivity, and grouping of wild pygmy chimpanzee females at Wamba, Zaire. Primates, 28(3), 309–318.

    Article  Google Scholar 

  • Furuichi, T. (1989). Social interactions and the life history of female Pan paniscus in Wamba, Zaire. International Journal of Primatology, 10, 173–197.

    Article  Google Scholar 

  • Furuichi, T., Idani, G., Ihobe, H., Kuroda, S., Kitamura, K., Mori, A., Enomoto, T., Okayasu, N., Hashimoto, C., & Kano, T. (1998). Population dynamics of wild bonobos (Pan paniscus) at Wamba. International Journal of Primatology, 19(6), 1029–1043.

    Article  Google Scholar 

  • Galdikas, B. M. F., & Wood, J. W. (1990). Birth spacing patterns in humans and apes. American Journal of Physical Anthropology, 83, 185–191.

    Article  PubMed  CAS  Google Scholar 

  • Geissmann, T. (2007). Status reassessment of gibbons: results of the Asian Primate Red List Workshop 2006. Gibbon Journal, 3, 5–15.

    Google Scholar 

  • Gintis, H. (2011). Gene–culture coevolution and the nature of human sociality. Philosophical Transactions of the Royal Society of London B: Biological Sciences, 366, 878–888.

    Article  Google Scholar 

  • Gittins, S. P. (1982). Feeding and ranging in the agile gibbon. Folia Primatologica, 38, 39–71.

    Article  CAS  Google Scholar 

  • Gittins, S., & Tilson, R. (1984). Notes on the ecology and behaviour of the hoolock gibbon. In H. Preuschoft, D. Chivers, W. Y. Brockelman, & N. Creel (Eds.), The lesser apes: Evolutionary and behavioural biology (pp. 258–266). Edinburgh: Edinburgh University Press.

    Google Scholar 

  • Goldsmith, M. L. (1996). Ecological influences on the ranging and grouping behaviour of western lowland gorillas at Bai Hoko¨u, Central African Republic. Ph.D. dissertation, State University of New York, Stony Brook.

  • Goodall, J. (1968). The behaviour of free-living chimpanzees in the Gombe Stream Reserve. Animal Behaviour Monographs, 1, 161–331.

    Google Scholar 

  • Goodall, J. (1986). The chimpanzees of Gombe: patterns of behaviour. Cambridge: Harvard University Press.

    Google Scholar 

  • Groves, C. P. (2001). Primate taxonomy. Washington: Smithsonian University Press.

    Google Scholar 

  • Haimoff, E. H., Yang, J. Y., He, S. J., & Chen, N. (1986). Census and survey of wild black crested gibbons (Hylobates concolor concolor). Folia Primatologica, 46, 205–214.

    Article  CAS  Google Scholar 

  • Haimoff, E., Yang, X. J., He, S. J., & Chen, N. (1987). Preliminary observations on black-crested gibbons (Hylobates concolor concolor) in Yunnan Province, People’s Republic of China. Primates, 28, 319–335.

    Article  Google Scholar 

  • Harcourt, A. H. (1979). Social relations among adult female mountain gorillas. Animal Behaviour, 27, 251–264.

    Article  Google Scholar 

  • Herrmann, E., Call, J., Hernandez-Lloreda, M. V., Hare, B., & Tomasello, M. (2007). Humans have evolved specialized skills of social cognition: the cultural intelligence hypothesis. Science, 317, 1360–1366.

    Article  PubMed  CAS  Google Scholar 

  • Hohmann, G., & Fruth, B. (2003). Lui Kotal—A new site for field research on bonobos in the Salonga National Park. Pan African News, 10, 25–27.

    Google Scholar 

  • Hohmann, G., & Fruth, B. (2008). New records on prey capture and meat eating by bonobos at Lui Kotale, Salonga National Park, Democratic Republic of Congo. Folia Primatologica, 79(2), 103–110.

    Article  Google Scholar 

  • Hohmann, G., Gerloff, U., Tautz, D., & Fruth, B. (1999). Social bonds and genetic ties: kinship, association and affiliation in a community of bonobos (Pan paniscus). Behaviour, 136(9), 1219–1235.

    Article  Google Scholar 

  • Hunt, K. D., & McGrew, W. C. (2002). Chimpanzees in the dry habitats of Assirik, Senegal and Semliki Wildlife Reserve, Uganda. In C. Boesch, G. Hohmann, & L. Marchant (Eds.), Behavioural diversity in chimpanzees and bonobos (pp. 35–51). New York: Cambridge University Press.

    Chapter  Google Scholar 

  • Inoue, E., Inoue-Murayama, M., Vigilant, L., Takenaka, O., & Nishida, T. (2008). Relatedness in wild chimpanzees: Influence of paternity, male philopatry, and demographic factors. American Journal of Physical Anthropology, 70, 62–68.

    Google Scholar 

  • Jablonka, E., & Lamb, M. (2005). Evolution in four dimensions: Genetic, epigenetic, behavioural, and symbolic variation in the history of life. Cambridge: Cambridge University Press.

    Google Scholar 

  • Jablonka, E., & Raz, G. (2009). Transgenerational epigenetic inheritance: Prevalance, mechanisms, and implications for the study of heredity and evolution. The Quarterly Review of Biology, 84(2), 131–176

    Google Scholar 

  • Jablonski, N. G., & Chaplin, G. (2009). The fossil record of gibbons. In S. Lappan & D. J. Whittaker (Eds.), The gibbons: New perspectives on small ape socioecology and population biology (pp. 111–130). New York: Springer.

    Google Scholar 

  • Jiang, X., Wang, Y., & Wang, Q. (1999). Coexistence of monogamy and polygyny in black crested gibbons (Hylobates concolor). Primates, 40, 607–611.

    Article  Google Scholar 

  • Kamilar, J. M., & Ledogar, J. A. (2011). Species co-occurrence patterns and dietary resource competition in primates. American Journal of Physical Anthropology, 144(1), 131–139.

    Article  PubMed  Google Scholar 

  • Kano, T. (1992). The last ape: Pygmy chimpanzee behaviour and ecology. Stanford: Stanford University Press.

    Google Scholar 

  • Kappeler, M. (1984). Vocal bouts and territorial maintenance in the moloch gibbon. In H. Prueschoft, D. Chivers, W. Y. Brockelman, & N. Creel (Eds.), The lesser apes: Evolution, behaviour, and biology (pp. 376–389). Edinburgh: Edinburgh University Press.

    Google Scholar 

  • Kelley, J. (1997). Paleobiological and phylogenetic significance of life history in Miocene hominoids. In D. R. Begun, C. V. Ward, & M. D. Rose (Eds.), Function, phylogeny, and fossils: Miocene hominoid evolution and adaptations (pp. 173–208). New York: Plenum Press.

    Google Scholar 

  • Kendal, J., Tehrani, J. J., & Odling-Smee, J. (2011). Human niche construction in interdisciplinary focus. Philosophical Transactions of the Royal Society of London B: Biological Sciences, 366, 785–792.

    Article  Google Scholar 

  • Knott, C. D. (1999a). Orangutan behaviour and ecology. In P. Dolhinow & A. Fuentes (Eds.), The nonhuman primates (pp. 50–57). Mountain View: Mayfield Publishing Company.

    Google Scholar 

  • Knott, C. D. (1999b). Reproductive, physiological and behavioural responses of orangutans in Borneo to fluctuations in food availability. Ph.D. thesis, Harvard University.

  • Knott, C. D., Beaudrot, L., Snaith, T., White, S., Tschauner, H., & Planansky, G. (2008). Female-female competition in Bornean orangutans. International Journal of Primatology, 29, 975–997.

    Article  Google Scholar 

  • Knott, C. D., & Kahlenberg, S. (2007). Orangutans in perspective: Forced copulations and female mating resistance. In C. J. Campbell, A. Fuentes, K. C. Mackinnon, M. Panger, & S. Bearder (Eds.), Primates in perspective (pp. 290–305). Oxford: Oxford University Press.

    Google Scholar 

  • Koenig, A., & Borries, C. (2009). The lost dream of ecological determinism: time to say goodbye?…Or a White Queen‘s proposal? Evolutionary Anthropology, 18, 166–174.

    Article  Google Scholar 

  • Laland, K. N., Odling-Smee, J., & Feldman, M. W. (2001). Niche construction, ecological Inheritance, and cycles of contingency in evolution. In S. Oyama, P. E. Griffiths, & R. D. Gray (Eds.), Cycles of contingency: Developmental systems and evolution (pp. 117–126). Cambridge: MIT Press.

    Google Scholar 

  • Lan, D., & Sheeran, L. K. (1995). The status of black gibbons (Hylobates concolor jingdongensis) at Xiaobahe, Wuliang Mountains, Yunnan Province, China. Asian Primates, 5, 2–4.

    Google Scholar 

  • Lappan, S. (2005). Biparental care and male reproductive strategies in siamangs (Symphalangus syndactylus) in southern Sumatra. PhD. thesis, New York University.

  • Lappan, S. (2007). Social relationships among males in multimale siamang groups. International Journal of Primatology, 28, 369–387.

    Article  Google Scholar 

  • Lappan, S., & Whittaker, D. J. (Eds.). (2009). The Gibbons: New perspectives on small ape socioecology and population biology. New York: Springer.

    Google Scholar 

  • Lehmann, J., & Boesch, C. (2008). Sexual differences in chimpanzee sociality. International Journal of Primatology, 29(1), 65–81.

    Article  PubMed  Google Scholar 

  • Leigh, S. R., & Shea, B. T. (1995). Ontogeny and the evolution of adult body size dimorphism in apes. American Journal of Primatology, 36, 37–60.

    Article  Google Scholar 

  • Leighton, D. L. (1987). Gibbons: Territoriality and monogamy. In B. Smuts, D. L. Cheney, R. M. Seyfarth, R. W. Wrangham, & T. T. Struhsaker (Eds.), Primate societies (pp. 135–145). Chicago: University of Chicago Press.

    Google Scholar 

  • MacKinnon, K. C., & Fuentes, A. (2011). Primates, niche construction, and social complexity: The roles of social cooperation and altruism. In: R. W. Sussman, & R. C. Cloninger (Eds.), Origins of altruism and cooperation (pp. 121–143). Developments in Primatology: Progress and Prospects, Vol. 36, Part 2. New York: Springer.

  • MacKinnon, J. R., & MacKinnon, K. S. (1980). Niche differentiation in a primate community. In D. J. Chivers (Ed.), Malayan forest primates: Ten year study in tropical rain forest (pp. 167–191). New York: Plenum Press.

    Google Scholar 

  • Maggioncalda, A. N., Sapolsky, R. M., & Czekala, N. M. (2002). Male orangutan subadulthood: a new twist on the relationship between chronic stress and developmental arrest. American Journal of Physical Anthropology, 118, 25–32.

    Article  PubMed  Google Scholar 

  • Malenky, R. K. (1990). Ecological factors affecting food choice and social organization in Pan paniscus. Ph.D. dissertation, State University of New York, Stony Brook.

  • Malone, N. M., & Fuentes, A. (2009). The ecology and evolution of hylobatid communities: Causal and contextual factors underlying inter- and intraspecific variation. In S. Lappan & D. J. Whittaker (Eds.), The gibbons: New perspectives on small ape socioecology and population biology (pp. 241–264). New York: Springer.

    Google Scholar 

  • McGrew, W. C. (1992). Chimpanzee material culture. Cambridge: Cambridge University Press.

    Book  Google Scholar 

  • Mootnick, A. R., Haimoff, E. H., & Nyunt-Lwin, K. (1987). Conservation and captive management of hoolock gibbons in the Socialist Republic of the Union of Burma. AAZPA 1987 Annual Proceedings, pp. 398–423.

  • Morin, P. A., Moore, J. J., Chakraborty, R., Jin, L., Goodall, J., & Woodruff, D. S. (1994). Kin selection, social structure, gene flow, and the evolution of chimpanzees. Science, 265, 1193–1200.

    Article  PubMed  CAS  Google Scholar 

  • Mukherjee, R. J., Chaudhuri, S., & Murmu, A. (1991–1992). Hoolock gibbons (Hylobates hoolock) in Arunachal Pradesh, Northeast India: The Lohit District. Primate Conservation, 12–13, 31–33.

    Google Scholar 

  • Myers Thompson, J. A. (2002). Bonobos of the Lukuru Wildlife Research Project. In C. Boesch, G. Hohmann, & L. Marchant (Eds.), Behavioural diversity in chimpanzees and bonobos (pp. 61–70). New York: Cambridge University Press.

    Chapter  Google Scholar 

  • Nishida, T. (1990). The chimpanzees of the Mahale Mountains: Sexual and life history strategies. Tokyo: University of Tokyo Press.

    Google Scholar 

  • Nishida, T., & Hiraiwa-Hasegawa, M. (1987). Chimpanzees and bonobos: Cooperative relationships among males. In B. B. Smuts, D. L. Cheney, R. M. Seyfarth, R. W. Wrangham, & T. T. Struhsaker (Eds.), Primate societies (pp. 165–177). Chicago: University of Chicago Press.

    Google Scholar 

  • Nishida, T., Uehara, S., & Nyundo, R. (1979). Predatory behaviour among wild chimpanzees of the Mahale Mountains. Primates, 20(1), 1–20.

    Article  Google Scholar 

  • Nowak, M. A., & Highfield, R. (2011). Supercooperators: Altruism, evolution, and why we need each other to succeed. New York: Free Press.

    Google Scholar 

  • Odling-Smee, J. (2007). Niche inheritance: a possible basis for classifying multiple inheritance systems in evolution. Biological Theory, 2(3), 276–289.

    Article  Google Scholar 

  • Odling-Smee, J., Laland, K. N., & Feldman, M. W. (2003). Niche construction: The neglected process in evolution. Princeton: Princeton University Press.

    Google Scholar 

  • Palombit, R. (1992). Pair bonds and monogamy in wild siamang (Hylobates syndactylus) and white-handed gibbon (Hylobates lar) in northern Sumatra. Ph.D. dissertation. University of California.

  • Palombit, R. (1994). Dynamic pair bonds in hylobatids: implications regarding monogamous social systems. Behaviour, 128(1–2), 65–101.

    Article  Google Scholar 

  • Palombit, R. (1996). Pair bonds in monogamous apes: a comparison of the siamang (Hylobates syndactylus) and the white-handed gibbon (Hylobates lar). Behaviour, 133, 321–356.

    Article  Google Scholar 

  • Palombit, R. A. (1997). Inter- and intraspecific variation in the diets of sympatric siamang (Hylobates syndactylus) and lar gibbons (Hylobates lar). Folia Primatologica, 68, 321–337.

    Article  CAS  Google Scholar 

  • Piersma, T., & Drent, J. (2003). Phenotypic flexibility and the evolution of organismal design. Trends in Ecology & Evolution, 18, 228–233.

    Article  Google Scholar 

  • Potts, R. (1998). Variability selection in human evolution. Evolutionary Anthropology, 7, 81–96.

    Article  Google Scholar 

  • Potts, R. (2004). Sociality and the concept of culture in human origins. In R. W. Sussman & A. R. Chapman (Eds.), The origins and nature of sociality (pp. 249–269). New York: Aldine de Gruyter.

    Google Scholar 

  • Pruetz, J. D. (2006). Feeding ecology of savanna chimpanzees (Pan troglodytes verus) at Fongoli, Senegal. In C. Boesch, G. Hohmann, & M. Robbins (Eds.), Feeding ecology in apes and other primates (pp. 161–182). Cambridge: Cambridge University Press.

    Google Scholar 

  • Raaum, R. L., Sterner, K. N., Noviello, C. M., Stewart, C. B., & Disotell, T. R. (2005). Catarrhine primate divergence dates estimated from complete mitochondrial genomes: concordance with fossil and nuclear DNA evidence. Journal of Human Evolution, 48, 237–257.

    Article  PubMed  Google Scholar 

  • Raemaekers, J. J. (1979). Ecology of sympatric gibbons. Folia Primatologica, 31, 227–245.

    Article  CAS  Google Scholar 

  • Ramachandran, V. S. (2011). The tell-tale brain: A neuroscientist’s quest for what makes us human. New York: W. W. Norton.

    Google Scholar 

  • Reichard, U. (1995). Extra-pair copulations in a monogamous gibbon (Hylobates lar). Ethology, 100, 99–112.

    Article  Google Scholar 

  • Reichard, U. (2003). Social monogamy in gibbons: the male perspective. In U. Reichard & C. Boesch (Eds.), Monogamy: Mating strategies and partnerships in birds, humans and other mammals (pp. 190–213). Cambridge: Cambridge University Press.

    Google Scholar 

  • Reichard, U. H. (2009). The social organization and mating system of Khao Yai white-handed gibbons (1992–2006). In S. Lappan & D. J. Whittaker (Eds.), The gibbons: New perspectives on small ape socioecology and population biology (pp. 347–384). New York: Springer.

    Google Scholar 

  • Reichard, U., & Barelli, C. (2008). Life history and reproductive strategies of Khao Yai white-handed gibbons (Hylobates lar): Implications for social evolution in apes. International Journal of Primatology, 29, 823–844.

    Article  Google Scholar 

  • Reynolds, V. (2005). The chimpanzees of the Budongo Forest: Ecology, behaviour, and conservation. Oxford: Oxford University Press.

    Book  Google Scholar 

  • Robbins, M. M. (2003). Behavioural aspects of sexual selection in mountain gorillas. In C. B. Jones (Ed.), Sexual selection and reproductive competition in primates: New perspectives and directions (pp. 477–501). American Society of Primatologists.

  • Robbins, M. M. (2007). Gorillas: Diversity in ecology and behaviour. In C. J. Campbell, A. Fuentes, K. C. Mackinnon, M. Panger, & S. Bearder (Eds.), Primates in perspective (pp. 305–321). Oxford: Oxford University Press.

    Google Scholar 

  • Robbins, M. M., Bermejo, M., Cipolletta, C., Magliocca, F., Parnell, R. J., & Stokes, E. (2004). Social structure and life history patterns in western gorillas (Gorilla gorilla gorilla). American Journal of Primatology, 64, 145–159.

    Article  PubMed  Google Scholar 

  • Robbins, M. M., Robbins, A. M., Gerald-Steklis, N., & Steklis, H. D. (2005). Long-term dominance relationships in female mountain gorillas: strength, stability, and determinants of rank. Behaviour, 142, 779–809.

    Article  Google Scholar 

  • Rogers, M. E., Abernethy, K., Bermejo, M., Cipolletta, C., Doran, D., McFarland, K., Nishihara, T., Remis, M., & Tutin, C. E. G. (2004). Western gorilla diet: a synthesis from six sites. American Journal of Primatology, 64, 173–192.

    Article  PubMed  Google Scholar 

  • Ruppell, J. (2007). The gibbons of Phong Nha-Ke Bang National Park in Vietnam. Gibbon Journal, 3, 50–54.

    Google Scholar 

  • Ruvolo, M. (1997). Genetic diversity in hominoid primates. Annual Review of Anthropology, 26, 515–540.

    Article  Google Scholar 

  • Sheeran, L. (1993). A preliminary study of the behvavior and socio-ecology of black gibbons (Hylobates concolor) in Yunnan Province, People’s Republic of China. PhD dissertation, University of Ohio, Columbus.

  • Sicotte, P. (1993). Inter-group encounters and female transfer in mountain gorillas: influence of group composition on male behaviour. American Journal of Primatology, 30, 21–36.

    Article  Google Scholar 

  • Sicotte, P. (1994). Effects of male competition on male-female relationships in bi-male groups of mountain gorillas. Ethology, 97, 47–64.

    Article  Google Scholar 

  • Siddiqi, N. A. (1986). Gibbons (Hylobates hoolock) in the West Bhanugach Reserved Forest of Sylhet District, Bangladesh. Tiger Paper, 8, 29–31.

    Google Scholar 

  • Srikosamatara, S. (1984). Ecology of pileated gibbons in south-east Thailand. In H. Prueschoft, D. Chivers, W. Y. Brockelman, & N. Creel (Eds.), The Lesser Apes: Evolution, behaviour, and biology (pp. 242–257). Edinburgh: Edinburgh University Press.

    Google Scholar 

  • Stamps, J. (2003). Behavioural processes affecting development: Tinbergen’s fourth question comes of age. Animal Behaviour, 66, 1–13.

    Article  Google Scholar 

  • Steiper, M. E. (2006). Population history, biogeography, and taxonomy of orangutans (Genus: Pongo) based on a population genetic meta-analysis of multiple loci. Journal of Human Evolution, 50, 509–522.

    Article  PubMed  Google Scholar 

  • Sterck, E. H. M., Watts, D. P., & van Schaik, C. P. (1997). The evolution of female social relationships in nonhuman primates. Behavioural Ecology and Sociobiology, 41, 291–309.

    Article  Google Scholar 

  • Sterelny, K. (2007). Social intelligence, human intelligence and niche construction. Philosophical Transactions of the Royal Society of London B: Biological Sciences, 362, 719–730.

    Article  Google Scholar 

  • Strier, K. B. (1994). Myth of the typical primate. Yearbook of Physical Anthropology, 37, 233–271.

    Article  Google Scholar 

  • Strier, K. B. (2003). Primatology comes of age: 2002 AAPA luncheon address. Yearbook of Physical Anthropology, 122, 2–13.

    Article  Google Scholar 

  • Strier, K. B. (2007). Primate behavioral ecology (3rd ed.). Boston: Allyn & Bacon.

    Google Scholar 

  • Stumpf, R. (2007). Chimpanzees and bonobos: Diversity within and between species. In C. J. Campbell, A. Fuentes, K. C. Mackinnon, M. Panger, & S. Bearder (Eds.), Primates in perspective (pp. 321–344). Oxford: Oxford University Press.

    Google Scholar 

  • Sugiyama, Y. (2004). Demographic parameters and life history of chimpanzees at Bossou, Guinea. American Journal of Physical Anthropology, 124(2), 154–165.

    Article  PubMed  Google Scholar 

  • Sugiyama, Y., & Koman, J. (1979). Social structure and dynamics of wild chimpanzees at Bossou, Guinea. Primates, 20, 323–339.

    Article  Google Scholar 

  • Sussman, R. W., & Cloninger, R. C. (2011). Origins of altruism and cooperation. Developments in Primatology: Progress and Prospects, Vol. 36, Part 2. New York: Springer.

  • Suwanvecho, U. (2003). Ecology and interspecific relations of tow sympatric Hylobates species (H. lar and H. pileatus) in Khao Yai National Park, Thailand. PhD thesis, Mahidol University, Bangkok, Thailand.

  • Thierry, B. (2008). Primate socioecology, the lost dream of ecological determinism. Evolutionary Anthropology, 17, 93–96.

    Article  Google Scholar 

  • Thinh, V. N., Mootnick, A. R., Thanh, V. N., Nadler, T., & Roos, C. (2010). A new species of crested gibbon from the central Annamite mountain range. Vietnamese Journal of Primatology, 4, 1–12.

    Google Scholar 

  • Tilson, R. L. (1979). Behaviour of hoolock gibbon (Hylobates hoolock) during different seasons in Assam, India. Journal of the Bombay Natural History Society, 79, 1–16.

    Google Scholar 

  • Tutin, C. E. G. (1996). Ranging and social structure of lowland gorillas in the Lopé Reserve, Gabon. In W. C. McGrew, L. F. Marchant, & T. Nishida (Eds.), Great ape societies (pp. 58–70). Cambridge: Cambridge University Press.

    Chapter  Google Scholar 

  • Tutin, C. E. G., & Fernandez, M. (1993). Composition of the diet of chimpanzees and comparisons with that of sympatric lowland gorillas in the Lope Reserve, Gabon. American Journal of Primatology, 30(3), 195–211.

    Article  Google Scholar 

  • Tyler, D. E. (1993). The evolutionary history of the gibbon. In N. Jablonski (Ed.), Evolving landscapes and evolving biotas of East Asia since the mid-Tertiary (pp. 228–240). Hong Kong: Center for Asian Studies, Hong Kong University.

    Google Scholar 

  • Utami, S. S., Wich, S. A., Sterck, E. H. M., & van Hooff, J. A. R. A. M. (1997). Food competition between wild orangutans in large fig trees. International Journal of Primatology, 18, 909–927.

    Article  Google Scholar 

  • van Schaik, C. P. (1999). The socioecology of fission-fusion sociality in orangutans. Primates, 40, 69–86.

    Article  Google Scholar 

  • van Schaik, C. P., Ancrenaz, M., Borgen, G., Galdikas, B., Knott, C., Singleton, I., Suzuki, A., Utami, S., & Merrill, M. (2003). Orangutan cultures and the evolution of material culture. Science, 299, 102–105.

    Article  PubMed  CAS  Google Scholar 

  • van Schaik, C. P., Preuschoft, S., & Watts, D. P. (2004). Great ape social systems. In A. E. Russon & D. R. Begun (Eds.), The evolution of thought: Evolutionary origins of great ape intelligence (pp. 335–345). Cambridge: Cambridge University Press.

    Google Scholar 

  • van Schaik, C. P., & van Hoof, J. A. R. A. M. (1983). On the ultimate causes of primate social systems. Behaviour, 85, 91–117.

    Article  Google Scholar 

  • Vigilant, L., & Bradley, B. J. (2004). Genetic variation in gorillas. American Journal of Primatology, 64, 161–172.

    Article  PubMed  CAS  Google Scholar 

  • Warren, K. S., Nijman, I. J., Lenstra, J. A., Swan, R. A., Heriyanto, & Den Boe, M. H. (2001). Speciation and intrasubspecific variation of Bornean orangutans, Pongo pygmaeus pygmaeus. Molecular Biology and Evolution, 18, 472–480.

    Article  PubMed  CAS  Google Scholar 

  • Watts, D. P. (1992). Social relationships of immigrant and resident female mountain gorillas. I. Male-female relationships. American Journal of Primatology, 28, 159–181.

    Article  Google Scholar 

  • Watts, D. P. (1996). Comparative socio-ecology of gorillas. In W. C. McGrew, L. F. Marchant, & T. Nishida (Eds.), Great ape societies (pp. 16–28). Cambridge: Cambridge University Press.

    Chapter  Google Scholar 

  • Watts, D. P. (2001). Female mountain gorillas: Social relationships. In: M. M. Robbins, P. Sicotte, & K. J. Stewart (Eds.), Mountain gorillas: Three decades of research at Karisoke (pp. 215–240). Cambridge Studies in Biological and Evolutionary Anthropology, Vol. 27. Cambridge, UK: Cambridge University Press.

  • Watts, D. P. (2008). Tool use by chimpanzees at Ngogo, Kibale National Park, Uganda. International Journal of Primatology, 29(1), 83–94.

    Article  Google Scholar 

  • Watts, D. P., & Mitani, J. C. (2002). Hunting and meat sharing by chimpanzees at Ngogo, Kibale National Park, Uganda. In C. Boesch, G. Hohmann, & L. Marchant (Eds.), Behavioural diversity in chimpanzees and bonobos (pp. 244–255). New York: Cambridge University Press.

    Chapter  Google Scholar 

  • West-Eberhardt, M. J. (2003). Developmental plasticity. Oxford: Oxford University Press.

    Google Scholar 

  • White, F. J. (1986). Behavioural ecology of the pygmy chimpanzee. Ph.D. dissertation, State University of New York, Stony Brook.

  • White, F. J. (1989). Social organization of pygmy chimpanzees. In P. G. Heltne & L. A. Marquardt (Eds.), Understanding chimpanzees (pp. 194–207). Cambridge: Harvard University Press.

    Google Scholar 

  • White, F. J. (1992). Activity budgets, feeding behaviour and habitat use of pygmy chimpanzees at Lomako, Zaire. American Journal of Primatology, 26, 215–223.

    Article  Google Scholar 

  • White, F. J. (1994). Food sharing in wild pygmy chimpanzees. In: J. R. Anderson, N. Herrenschmidt, J. J. Roeder, & B. Thierry (Eds.), Current primatology, Vol. II: Social development, learning and behaviour (pp.1–10). Proceedings of the 14th International Primatological Society Congress. Strasbourg, France: Universite Louis Pasteur.

  • White, F. J. (1996a). Pan paniscus 1973 to 1996: twenty-three years of field research. Evolutionary Anthropology, 5, 11–17.

    Article  Google Scholar 

  • White, F. J. (1996b). Importance of seasonality in great ape behaviour and ecology. IPS/ASP Congress Abstracts, 429.

  • White, F. J. (2008). Lomako bonobo population dynamics, habitat productivity, and the question of tool use. American Journal of Physical Anthropology, 46, 222.

    Google Scholar 

  • White, F. J., & Lanjouw, A. (1992). Feeding competition in Lomako bonobos: variation in social cohesion. Topics in Primatology, 1, 67–79.

    Google Scholar 

  • White, F. J., & Wrangham, R. W. (1988). Feeding competition and patch size in the chimpanzee species Pan paniscus and Pan troglodytes. Behaviour, 105, 148–163.

    Article  Google Scholar 

  • White, T. D., Asfaw, B., Beyene, Y., Haile-Selassie, Y., Lovejoy, C. O., Suwa, G., & WoldeGabriel, G. (2009). Ardipithecus ramidus and the paleobiology of early hominids. Science, 236, 75–86.

    Google Scholar 

  • Whiten, A., Goodall, J., McGrew, W. C., Nishida, T., Reynolds, V., Sugiyama, Y., Tutin, C. E., Wrangham, R. W., & Boesch, C. (1999). Chimpanzee cultures. Nature, 399, 682–685.

    Article  PubMed  CAS  Google Scholar 

  • Whitmore, T. C. (1984). Tropical rainforests of the Far East (2nd ed.). Oxford: Clarendon.

    Google Scholar 

  • Whittaker, D. J., & Lappan, S. (2009). The diversity of small apes and the importance of population-level studies. In S. Lappan & D. J. Whittaker (Eds.), The gibbons: New perspectives on small ape socioecology and population biology (pp. 3–10). New York: Springer.

    Google Scholar 

  • Whitten, A. J. (1984). Ecological comparisons between Kloss gibbons and other small gibbons. In H. Preuschoft, D. Chivers, W. Y. Brockelman, & N. Creel (Eds.), The lesser apes: Evolutionary and behavioural biology (pp. 219–227). Edinburgh: Edinburgh University Press.

    Google Scholar 

  • Wood, B., & Lonergan, N. (2008). The hominin fossil record: taxa, grades, and clades. Journal of Anatomy, 212, 354–376.

    Article  PubMed  Google Scholar 

  • Wood, B., & Richmond, B. (2000). Human evolution: taxonomy and paleobiology. Journal of Anatomy, 196, 19–60.

    Article  Google Scholar 

  • Wrangham, R. W. (1979). On the evolution of ape social systems. Social Science Information, 18, 335–369.

    Article  Google Scholar 

  • Wrangham, R. W. (1980). An ecological model of female-bonded primate groups. Behaviour, 75, 262–300.

    Article  Google Scholar 

  • Wrangham, R. W. (1986). Ecology and social relationships in two species of chimpanzee. In D. I. Rubenstein & R. W. Wrangahm (Eds.), Ecological aspects of social evolution: Birds and mammals (pp. 352–378). Princeton: Princeton University Press.

    Google Scholar 

  • Wrangham, R. W., Chapman, C. A., Clark-Acadi, A. P., & Isabirye-Basuta, G. (1996). The social ecology of Kanyawara chimpanzees: Implications for understanding the costs of great ape groups. In W. C. McGrew, T. Nishida, & L. Marchant (Eds.), Great ape societies (pp. 45–57). Cambridge: Cambridge University Press.

    Chapter  Google Scholar 

  • Yamagiwa, J., & Basabose, A. K. (2006). Diet and seasonal changes in sympatric gorillas and chimpanzees at Kahuzi–Biega National Park. Primates, 47(1), 74–90.

    Article  PubMed  Google Scholar 

  • Yamagiwa, J., Kahekwa, J., & Basabose, A. K. (2003). Intra-specific variation in social organization of gorillas: implications for their social evolution. Primates, 44, 359–369.

    Article  PubMed  Google Scholar 

  • Zhenhe, L., Yongzu, Z., Haisheng, J., & Southwick, C. (1989). Population structure of Hylobates concolor in Bawanglin Nature Reserve, Hainan, China. American Journal of Primatology, 19, 247–254.

    Article  Google Scholar 

Download references

Acknowledgments

We thank Michael Plavcan and the late Charles Lockwood for organizing a brilliant symposium at the XXIIth Congress of the International Primatological Society (Edinburgh, UK, 2008), and inviting our participation in this special edition. We acknowledge the efforts of the editor, as well as two anonymous reviewers, whose thought-provoking commentary across multiple drafts greatly improved the quality of this manuscript. We thank the Department of Anthropology at the University of Auckland (N. Malone) and the Dean’s Office of the College of Arts and Letters at the University of Notre Dame (A. Fuentes) for supporting this research. This research was supported by NSF grants BNS-8311252, SBR-9600547, and BCS-0610233 and support from the Leakey Foundation (F. J. White). Chelsea Humphrey (Boston University) assisted in the production of the figures contained herein.

Author information

Authors and Affiliations

  1. Department of Anthropology, University of Auckland, Auckland, 1142, New Zealand

    N. Malone

  2. Department of Anthropology, University of Notre Dame, Notre Dame, IN, 46556, USA

    A. Fuentes

  3. Department of Anthropology, University of Oregon, Eugene, OR, 97403, USA

    F. J. White

Authors
  1. N. Malone
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A. Fuentes
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. F. J. White
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to N. Malone.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Malone, N., Fuentes, A. & White, F.J. Variation in the Social Systems of Extant Hominoids: Comparative Insight into the Social Behavior of Early Hominins. Int J Primatol 33, 1251–1277 (2012). https://doi.org/10.1007/s10764-012-9617-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10764-012-9617-0

Keywords

Search

Navigation