Social learning and evolution: The cultural intelligence hypothesis

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 366, Issue 1567, 2011, Pages 1008-1016

  van Schaik, Carel P ^a   Burkart, Judith M ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

Brain size; Cross fostering; Enculturation; Intelligence; Social deprivation; Social learning

Indexed keywords

BRAIN; COGNITION; EVOLUTION; HYPOTHESIS TESTING; LEARNING; PREDICTION; PRIMATE; SOCIAL BEHAVIOR; WILD POPULATION;

ANIMALIA; AVES; HOMINIDAE; MAMMALIA; PRIMATES;

ANIMAL; BRAIN; HISTOLOGY; INTELLIGENCE; LEARNING; PHYSIOLOGY; REVIEW; SOCIAL BEHAVIOR;

ANIMALS; BRAIN; INTELLIGENCE; LEARNING; SOCIAL BEHAVIOR;

EID: 79959533839     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2010.0304     Document Type: Review

References (105)

1. Byrne, R. W. 1995 The thinking ape: evolutionary origins of intelligence. Oxford, UK: Oxford University Press.
2. Geary, D. C. 2005 The origin of mind: evolution of brain, cognition, and general intelligence. Washington, DC: American Psychological Association.
3. Moll, H. & Tomasello, M. 2007 Cooperation and human cognition: the Vygotskian intelligence hypothesis. Phil. Trans. R. Soc. B 362, 639-648. (doi:10. 1098/rstb.2006.2000)
4. Tomasello, M. 1999 The cultural origins of human cognition. Cambridge, MA: Harvard University Press.
5. 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. (doi:10. 1126/science.1146282)
6. Savage-Rumbaugh, S., Fields, W. M., Segerdahl, P. & Rumbaugh, D. 2005 Culture prefigures cognition in Pan/Homo bonobos. Theoria 54, 311-328.
7. Boesch, C. 2007 What makes us human (homo sapiens)? The challenge of cognitive cross-species comparison. J. Comp. Psychol. 121, 227-240. (doi:10.1037/ 0735-7036.121.3.227)
8. Gardner, B. T. & Gardner, R. A. 1989 Prelinguistic development of children and chimpanzees. Hum. Evol. 4, 433-460. (doi:10.1007/BF02436294)
9. Wilson, A. C. 1991 From molecular evolution to body and brain evolution. In Perspectives on cellular regulation: from bacteria to cancer (eds J. Campisi & A. B. Pardee), pp. 331-340. New York, NY: J. Wiley & Sons.
10. van Schaik, C. P. 2004 Among orangutans: red apes and the rise of human culture. Cambridge, MA: Harvard University Press (Belknap).
11. van Schaik, C. P. 2006 Why are some animals so smart? Sci. Am. 294, 64-71. (doi:10.1038/scientificamerican0406-64)
12. Whiten, A. & van Schaik, C. P. 2007 The evolution of animal 'cultures' and social intelligence. Phil. Trans. R. Soc. B 362, 603-620. (doi:10.1098/rstb. 2006.1998)
13. Richerson, P. J., Boyd, R. & Henrich, J. 2010 Gene-culture coevolution in the age of genomics. Proc. Natl Acad. Sci. USA 107, 8985-8992. (doi:10.1073/pnas. 0914631107)
14. Reader, S. M. & Laland, K. N. 2002 Social intelligence, innovation and enhanced brain size in primates. Proc. Natl Acad. Sci. USA 99, 4436-4441. (doi:10.1073/ pnas.062041299)
15. Nishida, T. & Turner, L. A. 1996 Food transfer between mother and infant chimpanzees of the Mahale Mountains National Park, Tanzania. Intl J. Primatol. 17, 947-968. (doi:10.1007/BF02735296)
16. van Schaik, C. P., Deaner, R. O. & Merrill, M. Y. 1999 The conditions for tool use in primates: implications for the evolution of material culture. J. Hum. Evol. 36, 719-741. (doi:10.1006/jhev.1999.0304)
17. Lonsdorf, E. V., Eberly, L. E. & Pusey, A. E. 2004 Sex differences in learning in chimpanzees. Nature 428, 715-716. (doi:10.1038/428715a)
18. Jaeggi, A., Dunkel, L., van Noordwijk, M. A., Wich, S. A., Sura, A. A. L. & van Schaik, C. P. 2010 Social learning of diet and foraging skills by wild immature Bornean orangutans: implications for culture. Am. J. Primatol. 72, 62-71. (doi:10.1002/ajp.20752)
19. Boesch, C. & Boesch-Achermann, H. 2000 The chimpanzees of the Tai{dotless}̈forest: behavioral ecology and evolution. Oxford, UK: Oxford University Press.
20. van Schaik, C. P. 2009 Geographic variation in the behavior of wild great apes: is it really cultural? In The question of animal culture (eds K. N. Laland & B. G. Galef), pp. 70-98. Cambridge, MA: Harvard University Press.
21. Whiten, A., Goodall, J., McGrew, W. C., Nishida, T., Reynolds, V., Sugiyama, Y., Tutin, C. E. G., Wrangham, R. W. & Boesch, C. 1999 Cultures in chimpanzees. Nature 399, 682-685. (doi:10.1038/21415)
22. van Schaik, C. P., Ancrenaz, M., Borgen, G., Galdikas, B., Knott, C. D., Singleton, I., Suzuki, A., Utami, S. S. & Merrill, M. 2003 Orangutan cultures and the evolution of material culture. Science 299, 102-105. (doi:10.1126/ science.1078004)
23. van Schaik, C. P., van Noordwijk, M. A. & Wich, S. A. 2006 Innovation in wild Bornean orangutans (Pongo pygmaeus wurmbii). Behaviour 143, 839-876. (doi:10. 1163/156853906778017944)
24. van Schaik, C. P. 2003 Local traditions in orangutans and chimpanzees: social learning and social tolerance. In The biology of traditions: models and evidence (eds D. M. Fragaszy & S. Perry), pp. 297-328. Cambridge, UK: Cambridge University Press.
25. Rapaport, L. G. & Brown, R. B. 2008 Social influences on foraging behavior in young nonhuman primates: learning what, where, and how to eat. Evol. Anthropol. 17, 189-201. (doi:10.1002/evan.20180)
26. van Schaik, C. P. & Pradhan, G. R. 2003 A model for tool-use traditions in primates: implications for the evolution of culture and cognition. J. Hum. Evol. 44, 645-664. (doi:10.1016/S0047-2484(03)00041-1)
27. Ottoni, E. & Izar, P. 2008 Watching the best nutcrackers: what capuchin monkeys (Cebus apella) know about others' tool-using skills. Evol. Anthropol. 17, 171-178. (doi:10.1002/evan.20185)
28. Perry, S. 2009 Are non-human primates likely to exhibit cultural capacities like those of humans? In The question of animal culture (eds K. N. Laland & B. G. Galef), pp. 247-268. Cambrdige, MA: Harvard University Press.
29. Terkel, J. 1996 Cultural transmission of feeding behavior in the black rat (Rattus rattus). In Social learning in animals: the roots of cultures (eds C. M. Heyes Jr & B. G. Galef Jr,), pp. 17-48. San Diego, CA: Academic Press.
30. Box, H. O. 1984 Primate behavior and social ecology. London, UK: Chapman and Hall.
31. Valone, T. J. 2007 From eavesdropping on performance to copying the behavior of others: a review of public information use. Behav. Ecol. Sociobiol. 62, 1-14. (doi:10.1007/s00265-007-0439-6)
32. Whiten, A., Horner, V., Litchfield, C. A. & Marshall-Pescini, S. 2004 How do apes ape? Learn. Behav. 32, 36-52.
33. Byrne, R. W. 2002 Imitation of novel complex action: what does the evidence from animals mean? Adv. Study Behav. 31, 77-105. (doi:10.1016/S0065-3454(02)80006-7)
34. Caldwell, C. & Whiten, A. 2007 Social learning in monkeys and apes: cultural animals? In Primates in perspective (eds C. J. Campbell, A. Fuentes, K. C. MacKinnon, M. Panger & S. Bearder), pp. 652-664. Oxford, UK: Oxford University Press.
35. Subiaul, F. 2007 The imitation faculty in monkeys: evaluating its features, distribution and evolution. J. Anthropol. Sci. 85, 35-62.
36. Galef, B. G. 1995 Why behaviour patterns that animals learn socially are locally adaptive. Anim. Behav. 49, 1325-1334. (doi:10.1006/anbe.1995.0164)
37. Heyes, C. 1994 Social learning in animals: categories and mechanisms. Biol. Rev. 69, 702-731. (doi:10. 1111/j.1469-185X.1994.tb01506.x)
38. Boyd, R. & Richerson, P. J. 1985 Culture and the evolutionary process. Chicago, IL: University of Chicago Press.
39. Rendell, L. et al. 2010 Why copy others? Insights from the social learning strategies tournament. Science 328, 208-213. (doi:10.1126/science.1184719)
40. Bandura, A. 1977 Social learning theory. Englewood Cliffs, NJ: Prentice Hall.
41. Custance, D. M., Whiten, A. & Fredman, T. 2002 Social learning and primate reintroduction. Int. J. Primatol. 23, 479-499. (doi:10.1023/ A:1014961415219)
42. Byrne, R. W. 2007 Culture in great apes: using intricate complexity in feeding skills to trace the evolutionary origin of human technical prowess. Phil. Trans. R. Soc. B 362, 577-585. (doi:10.1098/rstb.2006.1996)
43. Kenward, B., Weir, A. A. S., Rutz, C. & Kacelnik, A. 2005 Tool manufacture by naive juvenile crows. Nature 433, 121. (doi:10.1038/433121a)
44. Krakauer, E. B. 2005 Development of aye-aye (Daubentonia madagascariensis) foraging skills: independent exploration and social learning. Durham, NC: Duke University.
45. Videan, E. N. 2006 Bed-building in capitve chimpanzees (Pan traglodytes): the importance of early rearing. Am. J. Primatol. 68, 745-751. (doi:10.1002/ ajp.20265)
46. Morimura, N. & Mori, Y. 2010 Effects of early rearing conditions on problem-solving skill in captive male chimpanzees (Pan troglodytes). Am. J. Primatol. 71, 1-8.
47. Burkart, J. M., Foglia, M. & Strasser, A. 2009 Trade-offs between social learning and individual innovativeness in common marmosets, Callithrix jacchus. Anim. Behav. 77, 1291-1301. (doi:10.1016/j.anbehav.2009.02.006)
48. Whiten, A., Horner, V. & de Waal, F. B. M. 2005 Conformity to cultural norms of tool use in chimpanzees. Nature 437, 737-740. (doi:10.1038/nature04047)
49. Sargent, B. & Mann, J. 2009 From social learning to culture: intrapopulation variation in bottlenose dolphins. In The question of animal culture (eds K. N. Laland & B. G. Galef), pp. 152-173. Cambridge, MA: Harvard University Press.
50. Galef, B. G. & Whiskin, E. E. 2001 Interaction of social and individual learning in food preferences of Norway rats. Anim. Behav. 62, 41-46. (doi:10.1006/anbe. 2000.1721)
51. Slagsvold, T. 2004 Cross-fostering of pied flycatchers (Ficedula hypoleuca) to heterospecific hosts in the wild: a study of sexual imprinting. Behaviour 141, 1079-1102. (doi:10.1163/1568539042664614)
52. Harris, M. P. 1970 Abnormal migration and hybridization of Larus argentatus and L. fuscus after interspecies fostering experiments. IBIS 112, 488-498. (doi:10.1111/j.1474-919X.1970.tb00820.x)
53. Rowley, I. & Chapman, G. 1986 Cross-fostering, imprinting and learning in two sympatric species of cockatoo. Behaviour 96, 1-16. (doi:10.1163/ 156853986X00180)
54. Slagsvold, T. & Wiebe, K. L. 2007 Learning the ecological niche. Proc. R. Soc. B 274, 19-23. (doi:10. 1098/rspb.2006.3663)
55. Hawkins, L. K. & Cranford, J. A. 1992 Long-term effects of intraspecific and interspecific cross-fostering on two species of Peromyscus. J. Mammal. 73, 802-807. (doi:10.2307/1382199)
56. De Waal, F. B. M. & Johanowicz, D. L. 1993 Modification of reconciliation behavior through social experience: an experiment with two macaque species. Child Develop. 64, 897-908. (doi:10.2307/1131225)
57. Taggart, D. A., Schultz, D., White, C., Whitehead, P., Underwood, G. & Phillips, K. 2005 Cross-fostering, growth and reproductive studies in the brush-tailed wallaby, Petrogale penicillata (Marsupialia: Macropodidae): efforts to accelerate breeding in a threatened marsupial species. Aust. J. Zool. 53, 313-323. (doi:10.1071/ ZO05002)
58. Mason, W. A., Davenport, R. K. & Menzel, E. W. 1968 Early experience and the social development of rhesus monkeys and chimpanzees. In Early experience and behavior: the psychological and physiological effects of early environmental variaton (eds G. Newton & S. Levine), pp. 440-480. Springfield, IL: Charles C. Thomas.
59. Gilmer, W. S. & McKinney, W. T. 2003 Early experience and depressive disorders: human and non-human primate studies. J. Affect. Disord. 75, 97-113. (doi:10. 1016/S0165-0327(03)00046-6)
60. Smith, H. J. 2005 Parenting for primates. Cambridge, MA: Harvard University Press.
61. Ruppenthal, G. C., Arling, G. L., Harlow, H. F., Sackett, G. P. & Suomi, S. J. 1976 A 10-year perspective of motherless-mother monkey behavior. J. Abnorm. Psychol. 85, 341-349. (doi:10.1037/0021-843X.85.4.341)
62. Menzel, E. W., Davenport, R. K. & Rogers, C. M. 1970 The development of tool using in wild-born and restriction-reared chimpanzees. Folia Primatol. 12, 273-283. (doi:10.1159/000155297)
63. Fredman, T. & Whiten, A. 2008 Observational learning from tool using models by human-reared and motherreared capuchin monkeys (Cebus apella). Anim. Cogn. 11, 295-309. (doi:10.1007/s10071-007-0117-0)
64. Bjorklund, D. F. 2006 Mother knows best: epigenetic inheritance, maternal effects, and the evolution of human intelligence. Dev. Rev. 26, 213-242. (doi:10. 1016/j.dr.2006.02.007)
65. Tomasello, M. & Call, J. 2004 The role of humans in the cognitive development of apes revisited. Anim. Cogn. 7, 213-215. (doi:10.1007/s10071-004-0227-x)
66. Bard, K. A. & Gardner, K. H. 1996 Influences on development in infant chimpanzees: enculturation, temperament, and cognition. In Reaching into thought: the mind of great apes (eds A. Russon, K. Bard & S. T. Parker), pp. 235-255. Cambridge, UK: Cambridge University Press.
67. Call, J. & Tomasello, M. 1996 The effects of humans on the cognitive development of apes. In Reaching into thought: the mind of great apes (eds A. Russon, K. Bard & S. T. Parker), pp. 371-403. Cambridge, UK: Cambridge University Press.
68. Furlong, E., Boose, K. & Boysen, S. 2007 Raking it in: the impact of enculturation on chimpanzee tool use. Anim. Cogn. 11, 83-97. (doi:10.1007/s10071-007-0091-6)
69. Nisbett, R. E. 2009 Intelligence and how to get it: why schools and cultures count. New York, NY: W.W. Norton & Company.
70. Harlow, H. F. 1949 The formation of learning sets. Psychol. Rev. 56, 51-65. (doi:10.1037/h0062474)
71. Halsey, L. G., Bezerra, B. M. & Souto, A. S. 2006 Can wild common marmosets (Callithrix jacchus) solve the parallel strings task? Anim. Cogn. 9, 229-233. (doi:10. 1007/s10071-006-0016-9)
72. Laidre, M. E. 2008 Spontaneous performance of wild baboons on three novel food-access puzzles. Anim. Cogn. 11, 223-230. (doi:10.1007/s10071-007-0104-5)
73. Schrijver, N. C. A., Pallier, P. N., Brown, V. J. & Würbel, H. 2004 Double dissociation of social and environmental stimulation on spatial learning and reversal learning in rats. Behav. Brain Res. 152, 307-314. (doi:10.1016/j.bbr.2003.10.016)
74. Brent, L., Bloomsmith, M. A. & Fisher, S. D. 1995 Factors determining tool-using ability in two captive chimpanzee (Pan troglodytes) colonies. Primates 36, 265-274. (doi:10.1007/BF02381352)
75. Clarke, A. S. & Snipes, M. 1998 Early behavioral development and temperamental traits in mother-versus peer-reared rhesus monkeys. Primates 39, 433-448. (doi:10.1007/BF02557567)
76. Miles, H. L., Mitchell, R.W. & Harper, S. E. 1996 Simon says: the development of imitation in an enculturated orangutan. In Reaching into thought: the minds of the great apes (eds A. E. Russon, K. A. Bard & S. T. Parker), pp. 278-299. Cambridge, UK: Cambridge University Press.
77. Premack, D. 1983 The codes of man and beasts. Behav. Brain Sci. 6, 125-167. (doi:10.1017/ S0140525X00015077)
78. Finarelli, J. A. 2008 Testing hypotheses of the evolution of brain-body size scaling in the Canidae (Carnivora, Mammalia). Paleobiology 34, 35-45. (doi:10.1666/ 07030.1)
79. Reader, S. M., Hager, Y. & Laland, K. N. 2011 The evolution of primate general and cultural intelligence. Phil. Trans. R. Soc. B 366, 1017-1027. (doi:10.1098/ rstb.2010.0342)
80. Lefebvre, L. 2000 Feeding innovations and their cultural transmission in bird populations. In The evolution of cognition (eds C. Heyes & L. Huber), pp. 311-328. Cambridge, MA: MIT Press.
81. Martin, R. D. 1990 Primate origins and evolution; a phylogenetic reconstruction. London, UK: Chapman & Hall.
82. Masur, E. F. 1988 Infants' imitation of novel and familiar behaviors. In Social learning: psychological and biological perspectives (eds T. R. Zentall Jr & B. G. Galef Jr), pp. 301-318. Hillsdale, NJ: Erlbaum.
83. Coussi-Korbel, S. & Fragaszy, D. M. 1995 On the relation between social dynamics and social learning. Anim. Behav. 50, 1441-1453. (doi:10.1016/0003-3472(95)80001-8)
84. Deaner, R. O., Nunn, C. L. & van Schaik, C. P. 2000 Comparative tests of primate cognition: different scaling methods produce different results. Brain Behav. Evol. 55, 44-52. (doi:10.1159/000006641)
85. Dunbar, R. I. M. 1992 Neocortex size as a constraint on group size in primates. J. Hum. Evol. 20, 469-493. (doi:10.1016/0047-2484(92)90081-J)
86. Deaner, R. O., Isler, K., Burkart, J. M. & van Schaik, C. P. 2007 Overall brain size, and not encephalization quotient, best predicts cognitive ability across nonhuman primates. Brain Behav. Evol. 70, 115-124. (doi:10.1159/000102973)
87. Bennett, P. M. & Owens, I. P. F. 2002 Evolutionary ecology of birds: life histories, mating systems and extinction. Oxford, UK: Oxford University Press.
88. Wunderle Jr, J. M. 1991 Age-specific foraging proficiency in birds. Curr. Ornithol. 8, 273-324.
89. Iwaniuk, A. N. & Nelson, J. E. 2003 Developmental differences are correlated with relative brain size in birds: a comparative analysis. Can. J. Zool. 81, 1913-1928. (doi:10.1139/z03-190)
90. Madden, J. 2008 Do bowerbirds exhibit culture? Anim. Cogn. 11, 1-12. (doi:10.1007/s10071-007-0092-5)
91. Madden, J. 2001 Sex, bowers and brains. Proc. R. Soc. Lond. B 268, 833-838. (doi:10.1098/rspb.2000.1425)
92. Byrne, R. W. & Bates, L. A. 2007 Sociality, evolution and cognition. Curr. Biol. 17, R714-R723. (doi:10. 1016/j.cub.2007.05.069)
93. Stephan, H., Baron, G. & Frahm, H. D. 1988 Comparative size of brains and brain components. In Neurosciences: comparative primate biology, vol. 4 (eds H. D. Steklis & J. D. Erwin), pp. 1-38. New York, NY: Liss.
94. Dunbar, R. I. M. & Shultz, S. 2007 Evolution in the social brain. Science 317, 1344-1347. (doi:10.1126/ science.1145463)
95. Deaner, R. O., van Schaik, C. P. & Johnson, V. 2006 Do some taxa have better domain-general cognition than others? A meta-analysis of non-human primate studies. Evol. Psychol. 4, 149-196.
96. Banerjee, K., Charbis, C. F., Johnson, V. E., Lee, J. J., Tsao, F. & Hauser, M. D. 2009 General intelligence in another primate: individual differences across cognitive task performance in a New World monkey (Saguinus oedipus). PLoS ONE 4, e5883. (doi:10.1371/ journal.pone.0005883)
97. Isler, K. & van Schaik, C. P. 2009 The expensive brain: a framework for explaining evolutionary changes in brain size. J. Hum. Evol. 57, 392-400. (doi:10.1016/j. jhevol.2009.04.009)
98. Isler, K. & van Schaik, C. P. 2006 Costs of encephalization: the energy trade-off hypothesis tested on birds. J. Hum. Evol. 51, 228-243. (doi:10.1016/j.jhevol. 2006.03.006)
99. Aiello, L. C. & Wheeler, P. 1995 The expensive tissue hypothesis: the brain and digestive system in human and primate evolution. Curr. Anthropol. 36, 199-221. (doi:10.1086/204350)
100. Emery, N. J. & Clayton, N. S. 2004 The mentality of crows: convergent evolution of intelligence in corvids and apes. Science 306, 1903-1907. (doi:10.1126/ science.1098410)
101. Poole, J. H. & Moss, C. J. 2008 Elephant sociality and complexity: the scientific evidence. In Never forgetting: elephants and ethics (eds C. Wemmer & C. A. Christen). Baltimore, MD: Johns Hopkins University Press.
102. Gergely, G., Egyed, K. & Kiraly, I. 2007 On pedagogy. Dev. Sci. 10, 139-146. (doi:10.1111/j.1467-7687. 2007.00576.x)
103. de Waal, F. B. M. & Ferrari, P. F. 2010 Towards a bottom-up perspective on animal and human cognition. Trends Cogn. Sci. 14, 201-207. (doi:10.1016/j. tics.2010.03.003)
104. Hrdy, S. 2009 Mothers and others: the evolutionary origins of mutual understanding. Cambridge, UK: Harvard University Press.
105. Burkart, J. M., Hrdy, S. B. & van Schaik, C. P. 2009 Cooperative breeding and human cognitive evolution. Evol. Anthropol. 18, 175-186. (doi:10.1002/evan. 20222)