International Journal of Primatology

, Volume 33, Issue 5, pp 1165–1193

A Papionin Multilevel Society as a Model for Hominin Social Evolution

Article
First Online:
Received:
Accepted:

Abstract

Multilevel societies are unique in their ability to facilitate the maintenance of strong and consistent social bonds among some individuals while allowing separation among others, which may be especially important when social and sexual bonds carry significant and reliable benefits to individuals within social groups. Here we examine the importance of social and sexual bonds in the multilevel society of hamadryas baboons (Papio hamadryas) and apply these principles to social evolution in Plio-Pleistocene hominins. The behavior, adaptations, and socioecology of baboons (Papio spp.) have long been recognized as providing an important comparative sample to elucidate the processes of human evolution, and the social system of hamadryas baboons in particular shares even more similarities with humans than that of other baboons. Here we draw parallels between processes during the evolution of hamadryas social organization and those characterizing late Pliocene or early Pleistocene hominins, most likely Homo erectus. The higher costs of reproduction faced by female Homo erectus, exacerbated by an increased reliance on difficult to acquire, nutrient-dense foods, are commonly thought to have been alleviated by a strengthening of male–female bonds (via male provisioning and the evolution of monogamy) or by the assistance of older, postreproductive females (via grandmothering). We suggest that both of these social arrangements could have been present in Plio-Pleistocene hominins if we assume the development of a multilevel society such as that in hamadryas baboons. The evolution of a multilevel society thus underlies the adaptive potential for the complexity that we see in modern human social organization.

Keywords

Social bonds Reproductive strategies Human social evolution Homo erectus Papio hamadryas Pair bonding Grandmother hypothesis 

References

  1. Abegglen, J.-J. (1984). On socialization in hamadryas baboons. London: Associated University Presses.Google Scholar
  2. Achenbach, G. G., & Snowdon, C. T. (2002). Costs of caregiving: Weight loss in captive adult male cotton-top tamarins (Saguinus oedipus) following the birth of infants. International Journal of Primatology, 23, 105–122.CrossRefGoogle Scholar
  3. Aiello, L. C. (1996). Hominine preadaptations for language and cognition. In: P. Mellars & K. Gibson (Eds.), Modelling the early human mind (pp. 89–99). Cambridge: McDonald Institute Monographs.Google Scholar
  4. Aiello, L. C., & Dunbar, R. I. M. (1993). Neocortex size, group size, and the evolution of language. Current Anthropology, 34, 184–193.CrossRefGoogle Scholar
  5. Aiello, L. C., & Key, C. (2002). Energetic consequences of being a Homo erectus female. American Journal of Human Biology, 14, 551–565.PubMedCrossRefGoogle Scholar
  6. Aiello, L. C., & Wells, J. C. K. (2002). Energetics and the evolution of the genus Homo. Annual Review of Anthropology, 31, 323–338.CrossRefGoogle Scholar
  7. Aiello, L. C., & Wheeler, P. (1995). The expensive tissue hypothesis. Current Anthropology, 36, 199–221.CrossRefGoogle Scholar
  8. Alberts, S. C., & Altmann, J. (1995). Balancing costs and opportunities: Dispersal in male baboons. American Naturalist, 145, 279–306.CrossRefGoogle Scholar
  9. Alberts, S. C., & Altmann, J. (2006). The evolutionary past and the research future: Environmental variation and life history flexibility in a primate lineage. In L. Swedell & S. R. Leigh (Eds.), Reproduction and fitness in baboons (pp. 277–303). New York: Springer.Google Scholar
  10. Aldrich-Blake, F. P. G., Bunn, T. K., Dunbar, R. I. M., & Headley, P. M. (1971). Observations on baboons, Papio anubis, in an arid region in Ethiopia. Folia Primatologica, 15, 1–35.CrossRefGoogle Scholar
  11. Alexander, R. D., & Noonan, K. M. (1979). Concealment of ovulation, parental care, and Human social evolution. In N. A. Chagnon & W. Irons (Eds.), Evolutionary biology and human social behavior (pp. 436–453). North Scituate, MA: Duxbury Press.Google Scholar
  12. Anderson, C. M. (1983). Levels of social organization and male–female bonding in the genus Papio. American Journal of Physical Anthropology, 60, 15–22.PubMedCrossRefGoogle Scholar
  13. Antón, S. C. (2003). Natural history of Homo erectus. Yearbook of Physical Anthropology, 46, 126–170.CrossRefGoogle Scholar
  14. Antón, S. C. (2008). Framing the question: Diet and evolution in early Homo. In C. Vinyard, M. J. Ravosa, & C. Wall (Eds.), Primate craniofacial function and biology (pp. 443–482). Amsterdam: Springer.CrossRefGoogle Scholar
  15. Antón, S. C., & Swisher, C. C. (2004). Early dispersals of Homo from Africa. Annual Review of Anthropology, 33, 271–296.CrossRefGoogle Scholar
  16. Antón, S. C., Leonard, W. R., & Robertson, M. L. (2002). An ecomorphological model of the initial hominid dispersal from Africa. Journal of Human Evolution, 43, 773–785.PubMedCrossRefGoogle Scholar
  17. Archie, E. A., Moss, C. J., & Alberts, S. C. (2006). The ties that bind: Genetic relatedness predicts the fission and fusion of social groups in wild African elephants. Proceedings of the Royal Society of London B: Biological Sciences, 273, 513–522.CrossRefGoogle Scholar
  18. Baab, K. L. (2008). The taxonomic implications of cranial shape variation in Homo erectus. Journal of Human Evolution, 54, 827–847.PubMedCrossRefGoogle Scholar
  19. Barton, R. (2000). Socioecology of baboons: The interaction of male and female strategies. In P. M. Kappeler (Ed.), Primate males: Causes and consequences of variation in group composition (pp. 97–107). Cambridge, UK: Cambridge University Press.Google Scholar
  20. Bedaso, Z., Wynn, J. G., Alemseged, Z., & Geraads, D. (2010). Paleoenvironmental reconstruction of the Asbole fauna (Busidima Formation, Afar, Ethiopia) using stable isotopes. Geobios, 43, 165–177.CrossRefGoogle Scholar
  21. Begun, D. J., & Walker, A. (1993). The endocast. In A. Walker & R. Leakey (Eds.), The Nariokotome Homo erectus skeleton (pp. 326–358). Cambridge, MA: Harvard University Press.Google Scholar
  22. Bercovitch, F. B. (1990). Female choice, male reproductive success, and the origin of one male groups in baboons. In M. Thiago de Mello, A. Whiten, & R. W. Byrne (Eds.), Baboons: Behaviour and ecology, use and care. Selected Proceedings of the XIIth Congress of the International Primatological Society (pp. 61–76). Brasilia, Brasil.Google Scholar
  23. Bercovitch, F. B. (2001). Reproductive ecology of Old World monkeys. In P. T. Ellison (Ed.), Reproductive ecology and human evolution (pp. 369–396). New York: Aldine de Gruyter.Google Scholar
  24. 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 of London B: Biological Sciences, 277, 3045–3053.CrossRefGoogle Scholar
  25. Bird, R. (1999). Cooperation and conflict: The behavioral ecology of the sexual division of labor. Evolutionary Anthropology, 8, 65–75.CrossRefGoogle Scholar
  26. Bobe, R., & Behrensmeyer, A. K. (2004). The expansion of grassland ecosystems in Africa in relation to mammalian evolution and the origin of the genus Homo. Palaeogeography, Palaeoclimatology, Palaeoecology, 207, 399–420.CrossRefGoogle Scholar
  27. Bramble, D. M., & Lieberman, D. E. (2004). Endurance running and the evolution of Homo. Nature, 432, 345–352.PubMedCrossRefGoogle Scholar
  28. Bromage, T. G., & Dean, M. C. (1985). Re-evaluation of the age at death of immature fossil hominids. Nature, 317, 525–527.PubMedCrossRefGoogle Scholar
  29. Byrne, R. W., & Whiten, A. (Eds.). (1988). Machiavellian intelligence: Social expertise and the evolution of intellect in monkeys, apes, and humans. Oxford: Oxford University Press.Google Scholar
  30. Cerling, T., Wynn, J., Andanje, S., Bird, M., Korir, D., Levin, N., Mace, W., Macharia, A., Quade, J., & Remien, C. (2011). Woody cover and hominin environments in the past 6 million years. Nature, 476, 51–56.PubMedCrossRefGoogle Scholar
  31. Chapais, B. (2008). Primeval kinship: How pair-bonding gave birth to human society. Cambridge, MA: Harvard University Press.Google Scholar
  32. Charnov, E. L., & Berrigan, D. (1993). Why do female primates have such long lifespans and so few babies? or Life in the slow lane. Evolutionary Anthropology, 1, 191–194.CrossRefGoogle Scholar
  33. Clutton-Brock, T. H., & Parker, G. A. (1995). Sexual coercion in animal societies. Animal Behaviour, 49, 1345–1365.CrossRefGoogle Scholar
  34. Codron, D., Lee-Thorp, J. A., Sponheimer, M., de Ruiter, D., & Codron, J. (2008). What insights can baboon feeding ecology provide for early hominin niche differentiation? International Journal of Primatology, 29, 757–772.CrossRefGoogle Scholar
  35. Colmenares, F. (1991a). Greeting behaviour between male baboons: Oestrus females, rivalry and negotiation. Animal Behaviour, 41, 49–60.CrossRefGoogle Scholar
  36. Colmenares, F. (1991b). Greeting, aggression, and coalitions between male baboons: Demographic correlates. Primates, 32, 453–463.CrossRefGoogle Scholar
  37. Colmenares, F. (1992). Clans and harems in a colony of hamadryas and hybrid baboons: Male kinship, familiarity and the formation of brother-teams. Behaviour, 121, 61–94.CrossRefGoogle Scholar
  38. Colmenares, F. (2004). Kinship structure and its impact on behavior in multi-level societies. In B. Chapais & C. M. Berman (Eds.), Kinship and behavior in primates (pp. 242–270). New York: Oxford University Press.Google Scholar
  39. Connor, R. C., Mann, J., Tyack, P. L., & Whitehead, H. (1998). Social evolution in toothed whales. Trends in Ecology & Evolution, 13, 228–232.CrossRefGoogle Scholar
  40. Copeland, S. R., Sponheimer, M., de Ruiter, D. J., Lee-Thorp, J. A., Codron, D., le Roux, P. J., Grimes, V., & Richards, M. P. (2011). Strontium isotope evidence for landscape use by early hominins. Nature, 474, 76–79.Google Scholar
  41. Coqueugniot, H., Hublin, J.-J., Veillon, F., Houët, F., & Jacob, T. (2004). Early brain growth in Homo erectus and implications for cognitive ability. Nature, 431, 299–302.PubMedCrossRefGoogle Scholar
  42. Darwin, C. R. (1871). The descent of man and selection in relation to sex. London: John Murray.CrossRefGoogle Scholar
  43. Deacon, T. W. (1997). The symbolic species. New York: W. W. Norton.Google Scholar
  44. Dean, M. C. (2006). Tooth microstructure tracks the pace of human life-history evolution. Proceedings of the Royal Society London B, 273, 2799–2808.Google Scholar
  45. Dean, M. C., & Smith, B. H. (2009). Growth and development of the Nariokotome youth, KNM-WT 15000. In F. E. Grine, J. G. Fleagle, & R. E. Leakey (Eds.), The first human: Origin and early evolution of the genus Homo (pp. 101–120). New York: Springer.CrossRefGoogle Scholar
  46. Dean, C., Leakey, M. G., Reid, D., Schrenk, F., Schwartz, G. T., Stringer, C., & Walker, A. (2001). Growth processes in teeth distinguish modern humans from Homo erectus and earlier hominins. Nature, 414, 628–631.PubMedCrossRefGoogle Scholar
  47. deMenocal, P. (2004). African climate change and faunal evolution during the Pliocene-Pleistocene. Earth and Planetary Science Letters, 220, 3–24.CrossRefGoogle Scholar
  48. DeVore, I., & Washburn, S. L. (1963). Baboon ecology and human evolution. In F. C. Howell & F. Bourlière (Eds.), African ecology and human evolution (pp. 335–367). Chicago: Aldine.Google Scholar
  49. Dominguez-Rodrigo, M., & Pickering, T. R. (2003). Early hominid hunting and scavenging: A zooarcheological review. Evolutionary Anthropology, 12, 275–282.CrossRefGoogle Scholar
  50. Dominguez-Rodrigo, M., Serrallonga, J., Juan-Tresserras, J., Alcala, L., & Luque, L. (2001). Woodworking activities by early humans: A plant residue analysis on Acheulian stone tools from Peninj (Tanzania). Journal of Human Evolution, 40, 289–299.PubMedCrossRefGoogle Scholar
  51. Dunbar, R. I. M. (1983). Relationships and social structure in gelada and hamadryas baboons. In R. A. Hinde (Ed.), Primate social relationships: An integrated approach (pp. 299–307). Sunderland, MA: Sinauer Associates.Google Scholar
  52. Dunbar, R. I. M. (1988). Primate social systems. Ithaca, NY: Cornell University Press.CrossRefGoogle Scholar
  53. Dunbar, R. I. M. (1992a). A model of the gelada socio-ecological system. Primates, 33, 69–83.CrossRefGoogle Scholar
  54. Dunbar, R. I. M. (1992b). Neocortex size as a constraint on group size in primates. Journal of Human Evolution, 22, 469–493.CrossRefGoogle Scholar
  55. Dunbar, R. I. M. (1998). The social brain hypothesis. Evolutionary Anthropology, 6, 178–190.CrossRefGoogle Scholar
  56. Dunbar, R., & Dunbar, P. (1975). Social dynamics of gelada baboons. Basel: S. Karger.Google Scholar
  57. Egeland, C. P., & Dominguez-Rodrigo, M. (2008). Taphonomic perspectives on hominid site use and foraging strategies during Bed II times at Olduvai Gorge, Tanzania. Journal of Human Evolution, 55, 1031–1052.PubMedCrossRefGoogle Scholar
  58. Ellison, P. T. (2008). Energetics, reproductive ecology, and human evolution. PaleoAnthropology, 2008, 172–200.Google Scholar
  59. Elton, S. (2006). Forty years on and still going strong: The use of hominin-cercopithecid comparisons in palaeoanthropology. Journal of the Royal Anthropological Institute (N.S.), 12, 19–38.CrossRefGoogle Scholar
  60. Emlen, S. T., & Oring, L. W. (1977). Ecology, sexual selection, and the evolution of mating systems. Science, 197, 215–223.PubMedCrossRefGoogle Scholar
  61. Fischer, J., & Zinner, D. (2011). Communication and cognition in primate group movement. International Journal of Primatology, 32, 1279–1295.PubMedCrossRefGoogle Scholar
  62. Fisher, H. (1983). The sex contract: The evolution of human behavior. New York: Quill.Google Scholar
  63. Foley, R. A. (1989). The evolution of hominid social behaviour. In V. Standen & R. A. Foley (Eds.), Comparative socioecology: The behavioural ecology of humans and other mammals (pp. 473–494). Oxford: Blackwell.Google Scholar
  64. Foley, R. A. (1996). An evolutionary and chronological framework for human social behaviour. In W. G. Runciman, J. Maynard Smith, & R. I. M. Dunbar (Eds.), Evolution of social behaviour patterns in primates and man. Oxford: Oxford University Press.Google Scholar
  65. Foley, R., & Gamble, C. (2009). The ecology of social transitions in human evolution. Philosophical Transactions of the Royal Society of London B: Biological Sciences, 364, 3267–3279.CrossRefGoogle Scholar
  66. Foley, R. A., & Lee, P. C. (1989). Finite social space, evolutionary pathways, and reconstructing hominid behavior. Science, New Series, 243, 901–906.Google Scholar
  67. Foley, R. A., & Lee, P. C. (1991). Ecology and energetics of encephalization in hominid evolution. Philosophical Transactions of the Royal Society of London B: Biological Sciences, 334, 223–232.CrossRefGoogle Scholar
  68. Franciscus, R. G., & Trinkaus, E. (1988). Nasal morphology and the emergence of Homo erectus. American Journal of Physical Anthropology, 75, 517–527.PubMedCrossRefGoogle Scholar
  69. Galat-Luong, A., Galat, G., & Hagell, S. (2006). The social and ecological flexibility of Guinea baboons: Implications for Guinea baboon social organization and male strategies. In L. Swedell & S. R. Leigh (Eds.), Reproduction and fitness in baboons: Behavioral, ecological, and life history perspectives (pp. 105–121). New York: Springer.CrossRefGoogle Scholar
  70. Graves, R. R., Lupo, A. C., McCarthy, R. C., Wescott, D. J., & Cunningham, D. L. (2010). Just how strapping was KNM-WT 15000? Journal of Human Evolution, 59, 542–554.PubMedCrossRefGoogle Scholar
  71. Grueter, C. C., Chapais, B., & Zinner, D. (2012). Evolution of multilevel social systems in nonhuman primates and humans. International Journal of Primatology, 33.Google Scholar
  72. Grüter, C. C., & Zinner, D. (2004). Nested societies: Convergent adaptations of baboons and snub-nosed monkeys? Primate Report, 70, 1–98.Google Scholar
  73. Gurven, M., & Walker, R. (2006). Energetic demand of multiple dependents and the evolution of slow human growth. Proceedings of the Royal Society of London B: Biological Sciences, 273, 835–841.CrossRefGoogle Scholar
  74. Hamilton, M. J., Milne, B. T., Walker, R. S., Burger, O., & Brown, J. H. (2007). The complex structure of hunter-gatherer social networks. Proceedings of the Royal Society of London B: Biological Sciences, 274, 2195–2202.CrossRefGoogle Scholar
  75. Hammond, R. L., Lawson Handley, L. J., Winney, B. J., Bruford, M. W., & Perrin, N. (2006). Genetic evidence for female-biased dispersal and gene flow in a polygynous primate. Proceedings of the Royal Society of London B: Biological Sciences, 273, 479–484.CrossRefGoogle Scholar
  76. Hapke, A., Zinner, D., & Zischler, H. (2001). Mitochondrial DNA variation in Eritrean hamadryas baboons. Behavioral Ecology and Sociobiology, 50, 483–492.CrossRefGoogle Scholar
  77. Harvati, K., Frost, S. R., & McNulty, K. P. (2004). Neanderthal taxonomy reconsidered: Implications of 3D primate models of intra- and interspecific differences. Proceedings of the National Academy of Sciences of the USA, 101, 1147–1152.PubMedCrossRefGoogle Scholar
  78. Hawkes, K., O’Connell, J. F., & Blurton Jones, N. G. (1997). Hadza women's time allocation, offspring provisioning, and the evolution of long postmenopausal life spans. Current Anthropology, 38, 551–577.CrossRefGoogle Scholar
  79. Hawkes, K., O’Connell, J. F., Blurton Jones, N. G., Alvarez, H., & Charnov, E. L. (2000). The grandmother hypothesis and human evolution. In L. Cronk, N. Chagnon, & W. Irons (Eds.), Adaptation and human behavior (pp. 237–258). New York: Aldine De Gruyter.Google Scholar
  80. Hill, R. A., Bentley, A., & Dunbar, R. I. M. (2008). Network scaling reveals consistent fractal pattern in hierarchical mammalian societies. Biology Letters, 4, 748–751.PubMedCrossRefGoogle Scholar
  81. Hrdy, S. B. (2009). Mothers and others: The evolutionary origins of mutual understanding. Cambridge, MA: Harvard University Press.Google Scholar
  82. Isaac, G. (1978). The food-sharing behaviour of proto-human hominids. Scientific American, 238, 90–108.PubMedCrossRefGoogle Scholar
  83. Isbell, L. A., & Van Vuren, D. (1996). Differential costs of locational and social dispersal and their consequences for female group-living primates. Behaviour, 133, 1–36.CrossRefGoogle Scholar
  84. Iwamoto, T. (1979). Feeding ecology. In M. Kawai (Ed.), Ecological and sociological studies of gelada baboons, vol. 16 (pp. 280–335). Basel: Karger.Google Scholar
  85. Jack, K. M., & Isbell, L. A. (2009). Dispersal in primates: Advancing an individualized approach (Preface to Special Issue). Behaviour, 146, 429–436.CrossRefGoogle Scholar
  86. Johnson, G. A. (1983). Decision-making organization and pastoral nomad camp size. Human Ecology, 11, 175–199.CrossRefGoogle Scholar
  87. Jolly, C. J. (1963). A suggested case of evolution by sexual selection in primates. Man, 222, 177–178.CrossRefGoogle Scholar
  88. Jolly, C. J. (1970). The seed-eaters: A new model of hominid differentiation based on a baboon analogy. Man, 5, 1–26.Google Scholar
  89. Jolly, C. J. (1993). Species, subspecies, and baboon systematics. In W. H. Kimbel & L. B. Martin (Eds.), Species, species concepts, and primate evolution (pp. 67–107). New York: Plenum Press.Google Scholar
  90. Jolly, C. J. (2001). A proper study for mankind: Analogies from the Papionin monkeys and their implications for human evolution. Yearbook of Physical Anthropology, 44, 177–204.CrossRefGoogle Scholar
  91. Jolly, C. J. (2009). Fifty years of looking at human evolution: Backward, forward, and sideways. Current Anthropology, 50, 187–199.PubMedCrossRefGoogle Scholar
  92. Kaplan, H., Hill, K., Lancaster, J., & Hurtado, A. M. (2000). A theory of human life history evolution: Diet, intelligence, and longevity. Evolutionary Anthropology, 9, 156–185.CrossRefGoogle Scholar
  93. Kawai, M., Dunbar, R., Ohsawa, H., & Mori, U. (1983). Social organization of gelada baboons: Social units and definitions. Primates, 24, 13–24.CrossRefGoogle Scholar
  94. Key, C. A. (2000). The evolution of human life history. World Archaeology, 31, 329–350.PubMedCrossRefGoogle Scholar
  95. Key, C. A., & Aiello, L. C. (1999). The evolution of social organization. In R. Dunbar, K. Chris, & C. Power (Eds.), The evolution of culture (pp. 15–33). Piscataway, NJ: Rutgers University Press.Google Scholar
  96. Key, C., & Aiello, L. C. (2000). A prisoner's dilemma model of the evolution of paternal care. Folia Primatologica, 71, 77–92.CrossRefGoogle Scholar
  97. Key, C. A., & Ross, C. (1999). Sex differences in energy expenditure in non-human primates. Proceedings of the Royal Society of London B: Biological Sciences, 266, 2479–2485.CrossRefGoogle Scholar
  98. Kingston, J. D. (2007). Early human evolutionary paleoecology. Yearbook of Physical Anthropology, 50, 20–58.CrossRefGoogle Scholar
  99. Kleiman, D. G. (1977). Monogamy in mammals. The Quarterly Review of Biology, 52, 39–69.PubMedCrossRefGoogle Scholar
  100. Krützen, M., Sherwin, W. B., Connor, R. C., Barré, L. M., Van de Casteele, T., Mann, J., & Brooks, R. (2003). Contrasting relatedness patterns in bottlenose dolphins (Tursiops sp.) with different alliance strategies. Proceedings of the Royal Society of London B: Biological Sciences, 270, 497–502.CrossRefGoogle Scholar
  101. Kudo, H., & Dunbar, R. I. M. (2001). Neocortex size and social network size in primates. Animal Behaviour, 62, 711–722.CrossRefGoogle Scholar
  102. Kummer, H. (1968). Social organization of hamadryas baboons: A field study. Chicago: University of Chicago Press.Google Scholar
  103. Kummer, H. (1971). Primate societies. Chicago: Aldine.Google Scholar
  104. Kummer, H. (1990). The social system of hamadryas baboons and its presumable evolution. In M. Thiago de Mello, A. Whiten, & R. W. Byrne (Eds.), Baboons: Behaviour and ecology, use and care. Selected Proceedings of the XIIth Congress of the International Primatological Society (pp. 43–60). Brasilia, Brasil.Google Scholar
  105. Kummer, H., Götz, W., & Angst, W. (1974). Triadic differentiation: An inhibitory process protecting pair bonds in baboons. Behaviour, 49, 62–87.PubMedCrossRefGoogle Scholar
  106. Laden, G., & Wrangham, R. (2005). The rise of the hominids as an adaptive shift in fallback foods: Plant underground storage organs (USOs) and australopith origins. Journal of Human Evolution, 49, 482–498.PubMedCrossRefGoogle Scholar
  107. Layton, R. H., O’Hara, S., & Bilsborough, A. (2012). Antiquity and social functions of multi-level social organisation among human hunter-gatherers. International Journal of Primatology, 33 Google Scholar
  108. 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
  109. Leakey, M. D. (1971). Olduvai Gorge: Excavations in Beds I and II, 1960–1963. Cambridge, UK: Cambridge University Press.Google Scholar
  110. Leonard, W. R., & Robertson, M. L. (1997). Comparative primate energetics and hominid evolution. American Journal of Physical Anthropology, 102, 265–281.PubMedCrossRefGoogle Scholar
  111. Leonard, W. R., Robertson, M. L., Snodgrass, J. J., & Kuzawa, C. W. (2003). Metabolic correlates of hominid brain evolution. Comparative Biochemistry and Physiology. Part A, Molecular & Integrative Physiology, 136, 5–15.CrossRefGoogle Scholar
  112. Lockwood, C. A., Menter, C. G., Moggi-Cecchi, J., & Keyser, A. W. (2007). Extended male growth in a fossil hominin species. Science, 318, 1443–1446.PubMedCrossRefGoogle Scholar
  113. Lovejoy, C. O. (1981). The origin of man. Science, 211, 341–350.PubMedCrossRefGoogle Scholar
  114. Lovejoy, C. O. (2009). Reexamining human origins in light of Ardipithecus ramidus. Science, 326, 74.CrossRefGoogle Scholar
  115. Marlowe, F. W. (2010). The Hadza: Hunter-gatherers of Tanzania. Berkeley: University of California Press.Google Scholar
  116. Marlowe, F. W., Berbesque, J. C., Barr, A., Barrett, C., Bolyanatz, A., Cardenas, J. C., Ensminger, J., Gurven, M., Gwako, E., Henrich, J., Henrich, N., Lesorogol, C., McElreath, R., & Tracer, D. (2008). More ‘altruistic’ punishment in larger societies. Proceedings of the Royal Society of London B: Biological Sciences, 275, 587–590.CrossRefGoogle Scholar
  117. Maryanski, A. (1996). African ape social networks: A blueprint for reconstructing early hominid social structure. In J. Steele & S. Shennan (Eds.), The archaeology of human ancestry (pp. 67–90). London: Routledge.Google Scholar
  118. Matsuda, I., Zhang, P., Swedell, L., Mori, U., Tuuga, A., Bernard, H., & Sueur, C. (2012). Comparisons of inter-individual relationships among non-human primates living in multi-level social systems. International Journal of Primatology, 33.Google Scholar
  119. McHenry, H. M. (1994). Behavioral ecological implications of early hominid body size. Journal of Human Evolution, 27, 77–87.CrossRefGoogle Scholar
  120. McHenry, H. M. (1996). Sexual dimorphism in fossil hominids and its socioecological implications. In J. Steele & S. Shennan (Eds.), The archaeology of human ancestry (pp. 91–109). London: Routledge.Google Scholar
  121. McHenry, H. M., & Coffing, K. (2000). Australopithecus to Homo: Transformations in body and mind. Annual Review of Anthropology, 29, 125–146.CrossRefGoogle Scholar
  122. Milton, K. (1999). A hypothesis to explain the role of meat-eating in human evolution. Evolutionary Anthropology, 8, 11–21.CrossRefGoogle Scholar
  123. Mitani, J. C., Watts, D. P., & Muller, M. N. (2002). Recent developments in the study of wild chimpanzee behavior. Evolutionary Anthropology, 11, 9–25.CrossRefGoogle Scholar
  124. Monahan, C. M. (1996). New zooarchaeological data from Bed II, Olduvai Gorge, Tanzania: Implications for hominid behavior in the Early Pleistocene. Journal of Human Evolution, 31, 93–128.CrossRefGoogle Scholar
  125. Nunn, C. L. (1999). The number of males in primate social groups: A comparative test of the socioecological model. Behavioral Ecology and Sociobiology, 46, 1–13.CrossRefGoogle Scholar
  126. O’Connell, J. F., Hawkes, K., & Blurton Jones, N. G. (1999). Grandmothering and the evolution of Homo erectus. Journal of Human Evolution, 36, 461–485.PubMedCrossRefGoogle Scholar
  127. O’Connell, J. F., Hawkes, K., Lupo, K. D., & Blurton Jones, N. G. (2002). Male strategies and Plio-Pleistocene archaeology. Journal of Human Evolution, 43, 831–872.PubMedCrossRefGoogle Scholar
  128. Palombit, R. A. (2003). Male infanticide in wild savanna baboons: Adaptive significance and intraspecific variation. In C. B. Jones (Ed.), Sexual selection and reproductive competition in primates: New perspectives and directions (pp. 3–47). Norman, OK: The American Society of Primatologists.Google Scholar
  129. Pante, M. C. (2010). The larger mammal fossil assemblages from Beds III and IV, Olduvai Gorge, Tanzania: Implications for the feeding behavior of Homo erectus. Ph.D. thesis, Rutgers University.Google Scholar
  130. Parker, S. T. (1990). Why big brains are so rare: Energy costs of intelligence and brain size in anthropoid primates. In S. T. Parker & K. R. Gibson (Eds.), “Language” and intelligence in monkeys and apes (pp. 129–154). Cambridge, UK: Cambridge University Press.CrossRefGoogle Scholar
  131. Parker, S. T. (2004). The cognitive complexity of social organization and socialization in wild baboons and chimpanzees: Guided participation, socializing interactions, and event representation. In A. E. Russon & D. R. Begun (Eds.), The evolution of thought (pp. 45–60). Cambridge, UK: Cambridge University Press.CrossRefGoogle Scholar
  132. Patzelt, A., Zinner, D., Fickenscher, G., Diedhiou, S., Camara, B., Stahl, D., & Fischer, J. (2011). Group composition of Guinea baboons (Papio papio) at a water place suggests a fluid social organization. International Journal of Primatology, 32, 652–668.PubMedCrossRefGoogle Scholar
  133. Pereira, M. E. (1993). Juvenility in animals. In M. E. Pereira & L. A. Fairbanks (Eds.), Juvenile primates: Life history, development, and behavior (pp. 17–27). New York: Oxford University Press.Google Scholar
  134. Phillips-Conroy, J. E., Jolly, C. J., Nystrom, P., & Hemmalin, H. A. (1992). Migration of male hamadryas baboons into Anubis groups in the Awash National Park, Ethiopia. International Journal of Primatology, 13, 455–476.CrossRefGoogle Scholar
  135. Pines, M., & Swedell, L. (2011). Not without a fair fight: Failed abductions of females in wild hamadryas baboons. Primates, 52, 249–252.PubMedCrossRefGoogle Scholar
  136. Pines, M., Saunders, J., & Swedell, L. (2011). Alternative routes to the leader male role in a multi-level society: Follower versus solitary male strategies and outcomes in hamadryas baboons. American Journal of Primatology, 73, 679–691.PubMedCrossRefGoogle Scholar
  137. Plavcan, J. M. (1999). Mating systems, intrasexual competition and sexual dimorphism in primates. In P. C. Lee (Ed.), Comparative primate socioecology (pp. 241–260). Cambridge, UK: Cambridge University Press.CrossRefGoogle Scholar
  138. Plavcan, J. M. (2000). Inferring social behavior from sexual dimorphism in the fossil record. Journal of Human Evolution, 39, 327–344.PubMedCrossRefGoogle Scholar
  139. Plummer, T. (2004). Flaked stones and old bones: Biological and cultural evolution at the dawn of technology. Yearbook of Physical Anthropology, 47, 118–164.CrossRefGoogle Scholar
  140. Plummer, T. W., Ditchfield, P. W., Bishop, L. C., Kingston, J. D., Ferraro, J. V., Braun, D. R., Hertel, F., & Potts, R. (2009). Oldest evidence of tool-making hominins in a grassland-dominated ecosystem. PLoS One, 4, e7199.PubMedCrossRefGoogle Scholar
  141. Pobiner, B. L., Rogers, M. J., Monahan, C. M., & Harris, J. W. K. (2008). New evidence for hominin carcas processing strategies at 1.5 Ma, Koobi Fora, Kenya. Journal of Human Evolution, 55, 103–130.PubMedCrossRefGoogle Scholar
  142. Pontzer, H. (in press). Ecological energetics in early Homo. Current Anthropology Google Scholar
  143. Pontzer, H., & Kamilar, J. M. (2009). Greater ranging associated with greater reproductive investment in mammals. Proceedings of the National Academy of Sciences of the USA, 106, 102–106.CrossRefGoogle Scholar
  144. Potts, R. (1991). Why the Oldowan? Plio-Pleistocene toolmaking and the transport of resources. Journal of Anthropological Research, 47, 153–176.Google Scholar
  145. Potts, R. (1994). Variables versus models of early Pleistocene hominid land use. Journal of Human Evolution, 27, 7–24.CrossRefGoogle Scholar
  146. Potts, R. (1998). Environmental hypotheses of hominin evolution. Yearbook of Physical Anthropology, 41, 93–136.CrossRefGoogle Scholar
  147. Puts, D. A. (2010). Beauty and the beast: Mechanisms of sexual selection in humans. Evolution and Human Behavior, 31, 157–175.CrossRefGoogle Scholar
  148. Reed, K. E. (1997). Early hominid evolution and ecological change through the African Plio-Pleistocene. Journal of Human Evolution, 32, 289–322.PubMedCrossRefGoogle Scholar
  149. Ren, R., Garber, P. A., & Li, M. (2012). Fission–fusion behavior in Yunnan snub-nosed monkeys (Rhinopithecus bieti) in Yunnan, China. International Journal of Primatology, 33.Google Scholar
  150. Rodseth, L. (2012) From bachelor threat to fraternal security: Male associations and modular organization in human societies. International Journal of Primatology. doi:10.1007/s10764-012-9593-4.
  151. Rodseth, L., Wrangham, R. W., Harrigan, A. M., & Smuts, B. B. (1991). The human community as a primate society. Current Anthropology, 32, 221–254.CrossRefGoogle Scholar
  152. Rogers, M. J., Harris, J. W. K., & Feibel, C. S. (1994). Changing patterns of land use by Plio-Pleistocene hominids in the Lake Turkana Basin. Journal of Human Evolution, 27, 139–158.CrossRefGoogle Scholar
  153. Rose, M. D. (1976). Bipedal behavior of olive baboons (Papio anubis) and its relevance to an understanding of the evolution of human bipedalism. American Journal of Physical Anthropology, 44, 247–262.PubMedCrossRefGoogle Scholar
  154. Rubenstein, D. I. (2010). Ecology, social behavior, and conservation in zebras. Advances in the Study of Behavior, 42, 231–258.CrossRefGoogle Scholar
  155. Ruff, C. B. (2002). Variation in human body size and shape. Annual Review of Anthropology, 31, 211–232.CrossRefGoogle Scholar
  156. Ruff, C. B. (2008). Femoral/humeral strength in early African Homo erectus. Journal of Human Evolution, 54, 383–390.PubMedCrossRefGoogle Scholar
  157. Ruff, C. B. (2009). Relative limb strength and locomotion in Homo habilis. American Journal of Physical Anthropology, 138, 90–100.PubMedCrossRefGoogle Scholar
  158. Schick, K. D., & Toth, N. (1993). Making silent stones speak. New York: Simon and Schuster.Google Scholar
  159. Schreier, A. (2010). Feeding ecology, food availability and ranging patterns of wild hamadryas baboons at Filoha. Folia Primatologica, 81, 129–145.CrossRefGoogle Scholar
  160. Schreier, A., & Swedell, L. (2009). The fourth level of social structure in a multi-level society: Ecological and social functions of clans in hamadryas baboons. American Journal of Primatology, 71, 948–955.PubMedCrossRefGoogle Scholar
  161. Schreier, A., & Swedell, L. (2012a). The socioecology of network scaling ratios in the multilevel society of hamadryas baboons. International Journal of Primatology. doi:10.1007/s10764-011-9572-1.
  162. Schreier, A., & Swedell, L. (2012b). Ecology and sociality in a multilevel society: Ecological determinants of social cohesion in hamadryas baboons. American Journal of Physical Anthropology. doi:10.1002/ajpa.22076.
  163. Shultz, S., Opie, C., & Atkinson, Q. D. (2012). Stepwise evolution of stable sociality in primates. Nature, 479, 219–222.CrossRefGoogle Scholar
  164. Sigg, H., Stolba, A., Abegglen, J.-J., & Dasser, V. (1982). Life history of hamadryas baboons: Physical development, infant mortality, reproductive parameters and family relationships. Primates, 23, 473–487.CrossRefGoogle Scholar
  165. Sikes, N. E., Potts, R., & Behrensmeyer, A. K. (1999). Early Pleistocene habitat in Member 1 Olorgesailie based on paleosol stable isotopes. Journal of Human Evolution, 37, 721–746.PubMedCrossRefGoogle Scholar
  166. Silk, J. B. (2007a). The adaptive value of sociality in mammalian groups. Philosophical Transactions of the Royal Society of London B: Biological Sciences, 362, 539–559.CrossRefGoogle Scholar
  167. Silk, J. B. (2007b). Social components of fitness in primate groups. Science, 317, 1347–1351.PubMedCrossRefGoogle Scholar
  168. Silk, J. B., Beehner, J. C., Bergman, T. J., Crockford, C., Engh, A. L., Moscovice, L. R., Wittig, R. M., Seyfarth, R. M., & Cheney, D. L. (2009). The benefits of social capital: Close social bonds among female baboons enhance offspring survival. Proceedings of the Royal Society of London B: Biological Sciences, 276, 3099–3104.CrossRefGoogle Scholar
  169. Simpson, S. W., Quade, J., Levin, N. E., Butler, R., Dupont-Nivet, G., Everett, M., & Semaw, S. (2008). A female Homo erectus pelvis from Gona, Ethiopia. Science, 322, 1089–1092.PubMedCrossRefGoogle Scholar
  170. Smith, B. H., & Tompkins, R. L. (1995). Toward a life history of the hominidae. Annual Review of Anthropology, 24, 257–279.CrossRefGoogle Scholar
  171. Smolker, R., Richards, A. F., Connor, R. C., & Pepper, J. W. (1992). Sex differences in patterns of association among Indian Ocean bottlenose dolphins. Behaviour, 123, 38–69.CrossRefGoogle Scholar
  172. Smuts, B. B. (1985). Sex and Friendship in Baboons. New York, Aldine Publishing Company.Google Scholar
  173. Smuts, B. B., & Smuts, R. W. (1993). Male aggression and sexual coercion of females in nonhuman primates and other mammals: Evidence and theoretical implications. Advances in the Study of Behavior, 22, 1–63.CrossRefGoogle Scholar
  174. Snyder-Mackler, N., Beehner, J. C., & Bergman, T. J. (2012). Defining higher levels in a gelada multilevel society. International Journal of Primatology, 33.Google Scholar
  175. Strier, K. B. (1992). Atelinae adaptations: Behavioral strategies and ecological constraints. American Journal of Physical Anthropology, 88, 515–524.PubMedCrossRefGoogle Scholar
  176. Strier, K. B. (2001). Beyond the apes: Reasons to consider the entire primate order. In F. B. M. de Waal (Ed.), Tree of origin: What primate behavior can tell us about human social evolution (pp. 69–93). Cambridge, MA: Harvard University Press.Google Scholar
  177. Strum, S. C. (1987). Almost human. New York: W. W. Norton.Google Scholar
  178. Strum, S. C., & Mitchell, W. (1987). Baboon models and muddles. In W. G. Kinzey (Ed.), The evolution of human behavior: Primate models (pp. 87–104). Albany: State University of New York Press.Google Scholar
  179. Sueur, C., King, A. J., Conradt, L., Kerth, G., Lusseau, D., Mettke-Hofmann, C., Schaffner, C. M., Williams, L., Zinner, D., & Aureli, F. (2011). Collective decision-making and fission-fusion dynamics: A conceptual framework. Oikos, 120, 1608–1617.CrossRefGoogle Scholar
  180. Swedell, L. (2002). Affiliation among females in wild hamadryas baboons (Papio hamadryas hamadryas). International Journal of Primatology, 23, 1205–1226.CrossRefGoogle Scholar
  181. Swedell, L. (2006). Strategies of sex and survival in hamadryas baboons: Through a female lens. Upper Saddle River, NJ: Pearson Prentice Hall.Google Scholar
  182. Swedell, L. (2011). African Papionins: Diversity of social organization and ecological flexibility. In C. J. Campbell, A. Fuentes, K. C. MacKinnon, S. K. Bearder, & R. M. Stumpf (Eds.), Primates in perspective (2nd ed., pp. 241–277). New York: Oxford University Press.Google Scholar
  183. Swedell, L., & Saunders, J. (2006). Infant mortality, paternity certainty, and female reproductive strategies in hamadryas baboons. In L. Swedell & S. R. Leigh (Eds.), Reproduction and fitness in baboons (pp. 19–51). New York: Springer.Google Scholar
  184. Swedell, L., & Schreier, A. (2009). Male aggression towards females in hamadryas baboons: Conditioning, coercion, and control. In M. N. Muller & R. W. Wrangham (Eds.), Sexual coercion in primates and humans (pp. 244–268). Cambridge, MA: Harvard University Press.Google Scholar
  185. Swedell, L., & Tesfaye, T. (2003). Infant mortality after takeovers in wild Ethiopian hamadryas baboons. American Journal of Primatology, 60, 113–118.PubMedCrossRefGoogle Scholar
  186. Swedell, L., Hailemeskel, G., & Schreier, A. (2008). Composition and seasonality of diet in wild hamadryas baboons: Preliminary findings from Filoha. Folia Primatologica, 79, 476–490.CrossRefGoogle Scholar
  187. Swedell, L., Saunders, J., Schreier, A., Davis, B., Tesfaye, T., & Pines, M. (2011). Female “dispersal” in hamadryas baboons: Transfer among social units in a multilevel society. American Journal of Physical Anthropology, 145, 360–370.PubMedCrossRefGoogle Scholar
  188. Uchino, B. N. (2006). Social support and health: A review of physiological processes potentially underlying links to disease outcomes. Journal of Behavioral Medicine, 29, 377–387.PubMedCrossRefGoogle Scholar
  189. Ungar, P. S., Krueger, K. L., Blumenschine, R. J., Njau, J., & Scott, R. S. (2011). Dental microwear texture analysis of hominins recovered by the Olduvai Landscape Paleoanthropology Project, 1995–2007. Journal of Human Evolution. doi:10.1016/j.jhevol.2011.04.006.
  190. van der Merwe, N. J., Masao, F. T., & Bamford, M. K. (2008). Isotopic evidence for contrasting diets of early hominins Homo habilis and Australopithecus boisei of Tanzania. South African Journal of Science, 104, 153–155.Google Scholar
  191. van Schaik, C. P. (1983). Why are diurnal primates living in groups? Behaviour, 87, 120–144.CrossRefGoogle Scholar
  192. van Schaik, C. P., van Noordwijk, M. A., & Nunn, C. L. (1999). Sex and social evolution in primates. In P. C. Lee (Ed.), Comparative primate socioecology (pp. 204–231). Cambridge, UK: Cambridge University Press.CrossRefGoogle Scholar
  193. Vrba, E. S. (1985). Ecological and adaptive changes associated with early hominid evolution. In E. Delson (Ed.), Ancestors: The hard evidence (pp. 63–71). New York: Alan R. Liss.Google Scholar
  194. Vrba, E. S. (1988). Late Pliocene climatic events and hominid evolution. In F. E. Grine (Ed.), Evolutionary history of the “robust” australopithecines (pp. 405–426). New York: Aldine.Google Scholar
  195. Walker, A., & Ruff, C. (1993). The reconstruction of the pelvis. In A. Walker & R. Leakey (Eds.), The Nariokotome Homo erectus skeleton (pp. 221–233). Cambridge, MA: Harvard University Press.Google Scholar
  196. Washburn, S. L., & DeVore, I. (1961a). Social behavior of baboons and early man. In S. L. Washburn (Ed.), Social life of early man (pp. 91–105). Chicago: Aldine.Google Scholar
  197. Washburn, S. L., & DeVore, I. (1961b). The social life of baboons. Scientific American, 204, 62–71.CrossRefGoogle Scholar
  198. Wheeler, P. E. (1984). The evolution of bipedality and loss of functional body hair in hominids. Journal of Human Evolution, 13, 91–98.CrossRefGoogle Scholar
  199. Wittemyer, G., Douglas-Hamilton, I., & Getz, W. M. (2005). The socioecology of elephants: Analysis of the processes creating multitiered social structures. Animal Behaviour, 69, 1357–1371.CrossRefGoogle Scholar
  200. Wrangham, R. W. (1980). An ecological model of female-bonded primate groups. Behaviour, 75, 262–300.CrossRefGoogle Scholar
  201. Wrangham, R. W. (1987). The significance of African apes for reconstructing human social Evolution. In W. G. Kinzey (Ed.), The evolution of human behavior: Primate models (pp. 51–71). Albany: State University of New York Press.Google Scholar
  202. Wrangham, R., & Conklin-Brittain, N. (2003). Cooking as a biological trait. Comparative Biochemistry and Physiology A, 136, 35–46.CrossRefGoogle Scholar
  203. Wrangham, R., Holland Jones, J., Laden, G., Pilbeam, D., & Conklin-Brittain, N. L. (1999). The raw and the stolen: Cooking and the ecology of human origins. Current Anthropology, 40, 567–594.PubMedCrossRefGoogle Scholar
  204. Wrangham, R., Cheney, D., Seyfarth, R., & Sarmiento, E. (2009). Shallow-water habitats as sources of fallback foods for hominins. American Journal of Physical Anthropology, 140, 630–642.PubMedCrossRefGoogle Scholar
  205. Wright, S. (1931). Evolution in Mendelian populations. Genetics, 16, 97–259.PubMedGoogle Scholar
  206. Zhang, P., Watanabe, K., Li, B., & Tan, C. L. (2006). Social organization of Sichuan snub-nosed monkeys (Rhinopithecus roxellana) in the Qinling Mountains, Central China. Primates, 47, 374–382.PubMedCrossRefGoogle Scholar
  207. Zhang, P., Li, B., Qi, X., MacIntosh, A. J. J., & Watanabe, K. (2012). A proximity-based social network of the Sichuan snub-nosed monkey (Rhinopithecus roxellana). International Journal of Primatology, 33.Google Scholar
  208. Zihlman, A. L. (1978). Women in evolution, part II: Subsistence and social organization among early hominids. Signs, 4, 4–20.CrossRefGoogle Scholar
  209. Zihlman, A. L., & Tanner, N. M. (1978). Gathering and the hominid adaptation. In L. Tiger & H. T. Fowler (Eds.), Female hierarchies (p. 163). Chicago: Beresford Book Service.Google Scholar
  210. Zinner, D., Groeneveld, L. F., Keller, C., & Roos, C. (2009). Mitochondrial phylogeography of baboons (Papio spp.) – Indication for introgressive hybridization? BMC Evolutionary Biology, 9, 83.PubMedCrossRefGoogle Scholar
  211. Zuckerman, S. (1932). The social life of monkeys and apes. London: Routledge & Kegan Paul.Google Scholar
  212. Zuckerman, S., & Parkes, A. S. (1939). Observations on secondary sexual characters in monkeys. Journal of Endocrinology, 1, 430–439.CrossRefGoogle Scholar

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© Springer Science+Business Media, LLC 2012

Authors and Affiliations

  1. 1.Anthropology Department, Queens CollegeCity University of New YorkFlushingUSA
  2. 2.New York Consortium in Evolutionary PrimatologyNew YorkUSA

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