International Journal of Primatology

, Volume 33, Issue 6, pp 1251–1277

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

Article

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.

Keywords

Ecological and social niche construction Evolution Hominin social organization Hominoidea 

References

  1. Ahsan, F. (1995). Fighting between two females for a male in the Hoolock gibbon. International Journal of Primatology, 16, 731–737.CrossRefGoogle Scholar
  2. 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
  3. 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.Google Scholar
  4. 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.CrossRefGoogle Scholar
  5. 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.PubMedCrossRefGoogle Scholar
  6. Ashton, P. S. (1988). Dipterocarp biology as a window to the understanding of tropical forest structure. Annual Review of Ecological Systems, 19, 347–370.CrossRefGoogle Scholar
  7. 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.CrossRefGoogle Scholar
  8. 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.CrossRefGoogle Scholar
  9. 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
  10. Bartlett, T. Q. (2003). Intragroup and intergroup social interactions in white-handed gibbons. International Journal of Primatology, 24(2), 239–259.CrossRefGoogle Scholar
  11. 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
  12. 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
  13. 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.CrossRefGoogle Scholar
  14. Boesch, C. (1994). Cooperative hunting in wild chimpanzees. Animal Behaviour, 48, 653–667.CrossRefGoogle Scholar
  15. Boesch, C., & Boesch-Achermann, H. (2000). The chimpanzees of the Tai Forest: Behavioural ecology and evolution. New York: Oxford University Press.Google Scholar
  16. 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.PubMedCrossRefGoogle Scholar
  17. 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.CrossRefGoogle Scholar
  18. 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
  19. 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.CrossRefGoogle Scholar
  20. 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
  21. Chatterjee, H. J. (2006). Phylogeny and biogeography of gibbons: a dispersal-vicariance analysis. International Journal of Primatology, 27, 699–712.CrossRefGoogle Scholar
  22. 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
  23. Chivers, D. J. (1974). The siamang in Malaya: a field study of a primate in tropical rain forest. Contributions to Primatology, 4, 1–335.PubMedGoogle Scholar
  24. Choudhury, A. (1990). Population dynamics of Hoolock (Hylobates hoolock) in Assam, India. American Journal of Primatology, 20, 37–41.CrossRefGoogle Scholar
  25. 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.PubMedCrossRefGoogle Scholar
  26. Clutton-Brock, T. H. (1974). Primate social organization and ecology. Nature, 250, 539–542.CrossRefGoogle Scholar
  27. Clutton-Brock, T. H., & Harvey, P. H. (1977). Primate ecology and social organization. Journal of Zoology, 183(1), 1–39.CrossRefGoogle Scholar
  28. Conroy, G. C. (1990). Primate evolution. New York: W. W. Norton.Google Scholar
  29. 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.PubMedCrossRefGoogle Scholar
  30. 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
  31. 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.CrossRefGoogle Scholar
  32. Doran, D. M., & McNeilage, A. (1998). Gorilla ecology and behaviour. Evolutionary Anthropology, 6, 120–131.CrossRefGoogle Scholar
  33. Dunbar, R., Gamble, C., & Gowlett, J. (2010). Social brain, distributed mind. Proceedings of the British Academy, 158. New York, Oxford University Press.Google Scholar
  34. Dunbar, R. I. M., & Shultz, S. (2007). Evolution in the social brain. Science, 317, 1344–1347.PubMedCrossRefGoogle Scholar
  35. 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.PubMedCrossRefGoogle Scholar
  36. 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
  37. Ellefson, J. O. (1974). Natural history of white-handed gibbons in the Malayan peninsula. Ph.D. dissertation, University of California, Berkeley.Google Scholar
  38. 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
  39. 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.PubMedCrossRefGoogle Scholar
  40. Fleagle, J. G. (1999). Primate adaptation and evolution. San Diego: Academic.Google Scholar
  41. Fleming, T. H., Breitwisch, R., & Whitesides, G. H. (1987). Patterns of tropical vertebrate frugivore diversity. Annual Review of Ecological Systems, 18, 91–109.CrossRefGoogle Scholar
  42. 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.CrossRefGoogle Scholar
  43. Foley, R., & Lee, P. C. (1989). Finite social space, evolutionary pathways, and reconstructing hominid evolution. Science, 243, 901–906.PubMedCrossRefGoogle Scholar
  44. 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.CrossRefGoogle Scholar
  45. 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.PubMedCrossRefGoogle Scholar
  46. Fuentes, A. (2000). Hylobatid communities: changing views on pair bonding and social organization in hominoids. Yearbook of Physical Anthropology, 43, 33–60.CrossRefGoogle Scholar
  47. Fuentes, A. (2002). Patterns and trends in primate pair bonds. International Journal of Primatology, 23, 953–978.CrossRefGoogle Scholar
  48. Fuentes, A. (2009). Evolution of human behaviour. New York: Oxford University Press.Google Scholar
  49. 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
  50. 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.CrossRefGoogle Scholar
  51. Furuichi, T. (1987). Sexual swelling, receptivity, and grouping of wild pygmy chimpanzee females at Wamba, Zaire. Primates, 28(3), 309–318.CrossRefGoogle Scholar
  52. Furuichi, T. (1989). Social interactions and the life history of female Pan paniscus in Wamba, Zaire. International Journal of Primatology, 10, 173–197.CrossRefGoogle Scholar
  53. 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.CrossRefGoogle Scholar
  54. Galdikas, B. M. F., & Wood, J. W. (1990). Birth spacing patterns in humans and apes. American Journal of Physical Anthropology, 83, 185–191.PubMedCrossRefGoogle Scholar
  55. Geissmann, T. (2007). Status reassessment of gibbons: results of the Asian Primate Red List Workshop 2006. Gibbon Journal, 3, 5–15.Google Scholar
  56. 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.CrossRefGoogle Scholar
  57. Gittins, S. P. (1982). Feeding and ranging in the agile gibbon. Folia Primatologica, 38, 39–71.CrossRefGoogle Scholar
  58. 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
  59. 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.Google Scholar
  60. Goodall, J. (1968). The behaviour of free-living chimpanzees in the Gombe Stream Reserve. Animal Behaviour Monographs, 1, 161–331.Google Scholar
  61. Goodall, J. (1986). The chimpanzees of Gombe: patterns of behaviour. Cambridge: Harvard University Press.Google Scholar
  62. Groves, C. P. (2001). Primate taxonomy. Washington: Smithsonian University Press.Google Scholar
  63. 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.CrossRefGoogle Scholar
  64. 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.CrossRefGoogle Scholar
  65. Harcourt, A. H. (1979). Social relations among adult female mountain gorillas. Animal Behaviour, 27, 251–264.CrossRefGoogle Scholar
  66. 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.PubMedCrossRefGoogle Scholar
  67. 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
  68. 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.CrossRefGoogle Scholar
  69. 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.CrossRefGoogle Scholar
  70. 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.CrossRefGoogle Scholar
  71. 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
  72. 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
  73. 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), 131–176Google Scholar
  74. 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
  75. Jiang, X., Wang, Y., & Wang, Q. (1999). Coexistence of monogamy and polygyny in black crested gibbons (Hylobates concolor). Primates, 40, 607–611.CrossRefGoogle Scholar
  76. 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.PubMedCrossRefGoogle Scholar
  77. Kano, T. (1992). The last ape: Pygmy chimpanzee behaviour and ecology. Stanford: Stanford University Press.Google Scholar
  78. 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
  79. 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
  80. 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.CrossRefGoogle Scholar
  81. 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
  82. Knott, C. D. (1999b). Reproductive, physiological and behavioural responses of orangutans in Borneo to fluctuations in food availability. Ph.D. thesis, Harvard University.Google Scholar
  83. 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.CrossRefGoogle Scholar
  84. 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
  85. 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.CrossRefGoogle Scholar
  86. 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
  87. 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
  88. Lappan, S. (2005). Biparental care and male reproductive strategies in siamangs (Symphalangus syndactylus) in southern Sumatra. PhD. thesis, New York University.Google Scholar
  89. Lappan, S. (2007). Social relationships among males in multimale siamang groups. International Journal of Primatology, 28, 369–387.CrossRefGoogle Scholar
  90. Lappan, S., & Whittaker, D. J. (Eds.). (2009). The Gibbons: New perspectives on small ape socioecology and population biology. New York: Springer.Google Scholar
  91. Lehmann, J., & Boesch, C. (2008). Sexual differences in chimpanzee sociality. International Journal of Primatology, 29(1), 65–81.PubMedCrossRefGoogle Scholar
  92. 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.CrossRefGoogle Scholar
  93. 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
  94. 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.Google Scholar
  95. 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
  96. 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.PubMedCrossRefGoogle Scholar
  97. 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.Google Scholar
  98. 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
  99. McGrew, W. C. (1992). Chimpanzee material culture. Cambridge: Cambridge University Press.CrossRefGoogle Scholar
  100. 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.Google Scholar
  101. 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.PubMedCrossRefGoogle Scholar
  102. 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
  103. 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.CrossRefGoogle Scholar
  104. Nishida, T. (1990). The chimpanzees of the Mahale Mountains: Sexual and life history strategies. Tokyo: University of Tokyo Press.Google Scholar
  105. 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
  106. Nishida, T., Uehara, S., & Nyundo, R. (1979). Predatory behaviour among wild chimpanzees of the Mahale Mountains. Primates, 20(1), 1–20.CrossRefGoogle Scholar
  107. Nowak, M. A., & Highfield, R. (2011). Supercooperators: Altruism, evolution, and why we need each other to succeed. New York: Free Press.Google Scholar
  108. Odling-Smee, J. (2007). Niche inheritance: a possible basis for classifying multiple inheritance systems in evolution. Biological Theory, 2(3), 276–289.CrossRefGoogle Scholar
  109. Odling-Smee, J., Laland, K. N., & Feldman, M. W. (2003). Niche construction: The neglected process in evolution. Princeton: Princeton University Press.Google Scholar
  110. 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.Google Scholar
  111. Palombit, R. (1994). Dynamic pair bonds in hylobatids: implications regarding monogamous social systems. Behaviour, 128(1–2), 65–101.CrossRefGoogle Scholar
  112. 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.CrossRefGoogle Scholar
  113. 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.CrossRefGoogle Scholar
  114. Piersma, T., & Drent, J. (2003). Phenotypic flexibility and the evolution of organismal design. Trends in Ecology & Evolution, 18, 228–233.CrossRefGoogle Scholar
  115. Potts, R. (1998). Variability selection in human evolution. Evolutionary Anthropology, 7, 81–96.CrossRefGoogle Scholar
  116. 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
  117. 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
  118. 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.PubMedCrossRefGoogle Scholar
  119. Raemaekers, J. J. (1979). Ecology of sympatric gibbons. Folia Primatologica, 31, 227–245.CrossRefGoogle Scholar
  120. Ramachandran, V. S. (2011). The tell-tale brain: A neuroscientist’s quest for what makes us human. New York: W. W. Norton.Google Scholar
  121. Reichard, U. (1995). Extra-pair copulations in a monogamous gibbon (Hylobates lar). Ethology, 100, 99–112.CrossRefGoogle Scholar
  122. 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
  123. 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
  124. 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.CrossRefGoogle Scholar
  125. Reynolds, V. (2005). The chimpanzees of the Budongo Forest: Ecology, behaviour, and conservation. Oxford: Oxford University Press.CrossRefGoogle Scholar
  126. 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.Google Scholar
  127. 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
  128. 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.PubMedCrossRefGoogle Scholar
  129. 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.CrossRefGoogle Scholar
  130. 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.PubMedCrossRefGoogle Scholar
  131. Ruppell, J. (2007). The gibbons of Phong Nha-Ke Bang National Park in Vietnam. Gibbon Journal, 3, 50–54.Google Scholar
  132. Ruvolo, M. (1997). Genetic diversity in hominoid primates. Annual Review of Anthropology, 26, 515–540.CrossRefGoogle Scholar
  133. 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.Google Scholar
  134. 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.CrossRefGoogle Scholar
  135. Sicotte, P. (1994). Effects of male competition on male-female relationships in bi-male groups of mountain gorillas. Ethology, 97, 47–64.CrossRefGoogle Scholar
  136. Siddiqi, N. A. (1986). Gibbons (Hylobates hoolock) in the West Bhanugach Reserved Forest of Sylhet District, Bangladesh. Tiger Paper, 8, 29–31.Google Scholar
  137. 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
  138. Stamps, J. (2003). Behavioural processes affecting development: Tinbergen’s fourth question comes of age. Animal Behaviour, 66, 1–13.CrossRefGoogle Scholar
  139. 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.PubMedCrossRefGoogle Scholar
  140. 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.CrossRefGoogle Scholar
  141. Sterelny, K. (2007). Social intelligence, human intelligence and niche construction. Philosophical Transactions of the Royal Society of London B: Biological Sciences, 362, 719–730.CrossRefGoogle Scholar
  142. Strier, K. B. (1994). Myth of the typical primate. Yearbook of Physical Anthropology, 37, 233–271.CrossRefGoogle Scholar
  143. Strier, K. B. (2003). Primatology comes of age: 2002 AAPA luncheon address. Yearbook of Physical Anthropology, 122, 2–13.CrossRefGoogle Scholar
  144. Strier, K. B. (2007). Primate behavioral ecology (3rd ed.). Boston: Allyn & Bacon.Google Scholar
  145. 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
  146. Sugiyama, Y. (2004). Demographic parameters and life history of chimpanzees at Bossou, Guinea. American Journal of Physical Anthropology, 124(2), 154–165.PubMedCrossRefGoogle Scholar
  147. Sugiyama, Y., & Koman, J. (1979). Social structure and dynamics of wild chimpanzees at Bossou, Guinea. Primates, 20, 323–339.CrossRefGoogle Scholar
  148. 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.Google Scholar
  149. 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.Google Scholar
  150. Thierry, B. (2008). Primate socioecology, the lost dream of ecological determinism. Evolutionary Anthropology, 17, 93–96.CrossRefGoogle Scholar
  151. 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
  152. 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
  153. 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.CrossRefGoogle Scholar
  154. 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.CrossRefGoogle Scholar
  155. 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
  156. 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.CrossRefGoogle Scholar
  157. van Schaik, C. P. (1999). The socioecology of fission-fusion sociality in orangutans. Primates, 40, 69–86.CrossRefGoogle Scholar
  158. 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.PubMedCrossRefGoogle Scholar
  159. 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
  160. van Schaik, C. P., & van Hoof, J. A. R. A. M. (1983). On the ultimate causes of primate social systems. Behaviour, 85, 91–117.CrossRefGoogle Scholar
  161. Vigilant, L., & Bradley, B. J. (2004). Genetic variation in gorillas. American Journal of Primatology, 64, 161–172.PubMedCrossRefGoogle Scholar
  162. 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.PubMedCrossRefGoogle Scholar
  163. Watts, D. P. (1992). Social relationships of immigrant and resident female mountain gorillas. I. Male-female relationships. American Journal of Primatology, 28, 159–181.CrossRefGoogle Scholar
  164. 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.CrossRefGoogle Scholar
  165. 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.Google Scholar
  166. Watts, D. P. (2008). Tool use by chimpanzees at Ngogo, Kibale National Park, Uganda. International Journal of Primatology, 29(1), 83–94.CrossRefGoogle Scholar
  167. 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.CrossRefGoogle Scholar
  168. West-Eberhardt, M. J. (2003). Developmental plasticity. Oxford: Oxford University Press.Google Scholar
  169. White, F. J. (1986). Behavioural ecology of the pygmy chimpanzee. Ph.D. dissertation, State University of New York, Stony Brook.Google Scholar
  170. 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
  171. White, F. J. (1992). Activity budgets, feeding behaviour and habitat use of pygmy chimpanzees at Lomako, Zaire. American Journal of Primatology, 26, 215–223.CrossRefGoogle Scholar
  172. 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.Google Scholar
  173. White, F. J. (1996a). Pan paniscus 1973 to 1996: twenty-three years of field research. Evolutionary Anthropology, 5, 11–17.CrossRefGoogle Scholar
  174. White, F. J. (1996b). Importance of seasonality in great ape behaviour and ecology. IPS/ASP Congress Abstracts, 429.Google Scholar
  175. 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
  176. White, F. J., & Lanjouw, A. (1992). Feeding competition in Lomako bonobos: variation in social cohesion. Topics in Primatology, 1, 67–79.Google Scholar
  177. 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.CrossRefGoogle Scholar
  178. 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
  179. 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.PubMedCrossRefGoogle Scholar
  180. Whitmore, T. C. (1984). Tropical rainforests of the Far East (2nd ed.). Oxford: Clarendon.Google Scholar
  181. 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
  182. 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
  183. Wood, B., & Lonergan, N. (2008). The hominin fossil record: taxa, grades, and clades. Journal of Anatomy, 212, 354–376.PubMedCrossRefGoogle Scholar
  184. Wood, B., & Richmond, B. (2000). Human evolution: taxonomy and paleobiology. Journal of Anatomy, 196, 19–60.CrossRefGoogle Scholar
  185. Wrangham, R. W. (1979). On the evolution of ape social systems. Social Science Information, 18, 335–369.CrossRefGoogle Scholar
  186. Wrangham, R. W. (1980). An ecological model of female-bonded primate groups. Behaviour, 75, 262–300.CrossRefGoogle Scholar
  187. 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
  188. 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.CrossRefGoogle Scholar
  189. 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.PubMedCrossRefGoogle Scholar
  190. 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.PubMedCrossRefGoogle Scholar
  191. 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.CrossRefGoogle Scholar

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© Springer Science+Business Media, LLC 2012

Authors and Affiliations

  1. 1.Department of AnthropologyUniversity of AucklandAucklandNew Zealand
  2. 2.Department of AnthropologyUniversity of Notre DameNotre DameUSA
  3. 3.Department of AnthropologyUniversity of OregonEugeneUSA

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