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3 - Relative brain size and the distribution of innovation and social learning across the nonhuman primates

Published online by Cambridge University Press:  27 October 2009

Simon M. Reader
Affiliation:
Behavioural Biology, Utrecht University, Padualaan 14, PO Box 80086, 3508 TB, Utrecht, The Netherlands
Dorothy M. Fragaszy
Affiliation:
University of Georgia
Susan Perry
Affiliation:
University of California, Los Angeles
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Summary

The history of comparative learning could simply be classified as disappointing. The comparative psychologist often appears to know little more than the grade school child who would rather have a pet dog than bird, or bird than fish, or fish than worm, simply because they make better friends, as they can be taught more. This state of affairs did not arise without considerable effort.

Riddell, 1979, p. 95

Introduction

Ecology and “intelligence” are two commonly invoked explanations for species differences in the reliance on socially learned traditions, yet we know little about how social learning evolved. Here, I examine hypotheses for the evolution and evolutionary consequences of social learning and detail possible routes to address these ideas. I will test social and ecological hypotheses for primate brain evolution to illustrate possible approaches to the study of traditions. This chapter explores cognitive, ecological, and life-history variables that may accompany a propensity for social learning, specifically, the roles of brain size and social group size. I also examine the distribution of innovations and tool use across the nonhuman primates, to determine how these aspects of behavioral plasticity are associated with social learning and to explore the relationship between asocial and social learning. Such analyses can provide important clues as to whether we can sensibly talk about the “evolution of traditions”, or whether an increased reliance on social learning is simply a by-product of selection for generalized learning abilities.

Type
Chapter
Information
The Biology of Traditions
Models and Evidence
, pp. 56 - 93
Publisher: Cambridge University Press
Print publication year: 2003

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References

Aiello, L. C. and Dunbar, R. I. M. 1993. Neocortex size, group size and the evolution of language. Current Anthropology, 34, 184–193CrossRefGoogle Scholar
Ancel, L. W. 1999. A quantitative model of the Simpson–Baldwin effect. Journal of Theoretical Biology, 196, 197–209CrossRefGoogle ScholarPubMed
Baldwin, J. M. 1896. A new factor in evolution. American Naturalist, 30, 441–451, 536–553
Barton, R. A. 1993. Independent contrasts analysis of neocortical size and socioecology in primates. Behavioral and Brain Sciences, 16, 694–695CrossRefGoogle Scholar
Barton, R. A. 1996. Neocortex size and behavioural ecology in primates. Proceedings of the Royal Society of London, Series B, 263, 173–177CrossRefGoogle ScholarPubMed
Barton, R. 1999. The evolutionary ecology of the primate brain. In Comparative Primate Socioecology, ed. P. C. Lee, pp. 167–194. Cambridge: Cambridge University Press
Barton, R. A. and Dunbar, R. I. M. 1997. Evolution of the social brain. In Machiavellian Intelligence II, ed. A. Whiten, and R. W. Byrne, pp. 240–263. Cambridge: Cambridge University Press
Barton, R. A. and Harvey, P. H. 2000. Mosaic evolution of brain structure in mammals. Nature, 405, 1055–1058CrossRefGoogle ScholarPubMed
Barton, R. A. and Purvis, A. 1994. Primate brains and ecology: looking beneath the surface. In Current Primatology: Proceedings of the XIVth Congress of the International Primatological Society, ed. J. R. Anderson, B. Thierry, and N. Herrnschmidt, pp. 1–11. Strasbourg: Université Louis Pasteur
Barton, R. A., Purvis, A., and Harvey, P. H. 1995. Evolutionary radiation of visual and olfactory brain systems in primates, bats and insectivores. Philosophical Transactions of the Royal Society of London, Series B, 348, 381–392CrossRefGoogle ScholarPubMed
Bateson, P. P. G. 1983. Genes, environment and the development of behavior. In Animal Behavior, Vol. 3, Genes, Development and Learning, ed. T. R. Halliday, and P. J. B. Slater, pp. 52–81. Oxford: Blackwell
Bateson, P. G. 1988. The active role of behavior in evolution. In Evolutionary Processes and Metaphors, ed. M.-W. Ho, and S. W. Fox, pp. 191–207. Chicester: Wiley
Bateson, P. P. G. and Martin, P. 1999. Design for a Life: How Behavior Develops. London: Jonathan Cape
Bearder, S. K. 1987. Infants and adult males. In Primate Societies, ed. B. B. Smuts, D. L. Cheney, R. M. Seyfarth, R. W. Wrangham, and T. T. Struhsaker, pp. 11–24. Chicago, IL: University of Chicago Press
Beck, B. B. 1980. Animal Tool Behavior: The Use and Manufacture of Tools by Animals. New York: Garland
Boyd, R. and Richerson, P. J. 1985. Culture and the Evolutionary Process. Chicago, IL: University of Chicago Press
Boyd, R. and Richerson, P. J. 2000. Memes: universal acid or a better mousetrap. In Darwinizing Culture: The Status of Memetics as a Science, ed. R. Aunger, pp. 143–162. Oxford: Oxford University Press
Byrne, R. W. 1992. The evolution of intelligence. In Behaviour and Evolution, ed. P. J. B. Slater and T. R. Halliday, pp. 223–265. Cambridge: Cambridge University Press
Byrne, R. W. 1993. Do larger brains mean greater intelligence?Behavioral and Brain Sciences, 16, 696–697CrossRefGoogle Scholar
Byrne, R. W. 1997. The technical intelligence hypothesis: an additional evolutionary stimulus to intelligence? In Machiavellian Intelligence II, ed. A. Whiten and R. W. Byrne, pp. 289–311. Cambridge: Cambridge University Press
Byrne, R. W. and Whiten, A. 1992. Cognitive evolution: evidence from tactical deception. Man, 27, 609–627CrossRefGoogle Scholar
Byrne, R. W. and Whiten, A. 1997. Machiavellian intelligence. In Machiavellian Intelligence II, ed. A. Whiten and R. W. Byrne, pp. 1–23. Cambridge: Cambridge University Press
Byrne, R. W. and Whiten, A. 1988. Machiavellian Intelligence: Social Expertise and the Evolution of Intellect in Monkeys, Apes and Humans. Oxford: Oxford University Press
Cambefort, J. P. 1981. A comparative study of culturally transmitted patterns of feeding habits in the chacma baboon Papio ursinus and the vervet monkey Cercopithecus aethiops. Folia Primatologica, 36, 243–263CrossRefGoogle ScholarPubMed
Connor, R. C., Mann, J., and Tyack, P. L. 1998. Reply to Marino. Trends in Ecology and Evolution, 13, 408CrossRefGoogle Scholar
Deacon, T. W. 1993. Confounded correlations, again. Behavioral and Brain Sciences, 16, 698–699CrossRefGoogle Scholar
Deaner, R. O. and Nunn, C. L. 1999. How quickly do brains catch up with bodies? A comparative method for detecting evolutionary lag. Proceedings of the Royal Society of London, Series B, 266, 687–694CrossRefGoogle ScholarPubMed
Deaner, R. O., Nunn, C. L., and Schaik, C. P. 2000. Comparative tests of primate cognition: different scaling methods produce different results. Brain, Behavior and Evolution, 55, 44–52CrossRefGoogle ScholarPubMed
Dixson, A. F. 1998. Primate Sexuality: Comparative Studies of the Prosimians, Monkeys, Apes and Human Beings. Oxford: Oxford University Press
Dunbar, R. I. M. 1991. Functional significance of social grooming in primates. Folia Primatologica, 57, 121–131CrossRefGoogle Scholar
Dunbar, R. I. M. 1992. Neocortex size as a constraint on group size in primates. Journal of Human Evolution, 20, 469–493CrossRefGoogle Scholar
Dunbar, R. I. M. 1993a. On the origins of language: a history of constraints and windows of opportunity. Behavioral and Brain Sciences, 16, 721–729CrossRefGoogle Scholar
Dunbar, R. I. M. 1993b. Coevolution of neocortical size, group size and language in humans. Behavioral and Brain Sciences, 16, 681–735CrossRefGoogle Scholar
Dunbar, R. I. M. 1995. Neocortex size and group size in primates: a test of the hypothesis. Journal of Human Evolution, 28, 287–296CrossRefGoogle Scholar
Essock-Vitale, S. and Seyfarth, R. M. 1987. Intelligence and social cognition. In Primate Societies, ed. B. B. Smuts, D. L. Cheney, R. M. Seyfarth, R. W. Wrangham, and T. T. Struhsaker, pp. 452–461. Chicago, IL: University of Chicago Press
Feldman, M. W. and Laland, K. N. 1996. Gene–culture coevolutionary theory. Trends in Ecology and Evolution, 11, 453–457CrossRefGoogle ScholarPubMed
Felsenstein, J. 1985. Phylogenies and the comparative method. American Naturalist, 125, 1–15CrossRefGoogle Scholar
Fisher, J. and Hinde, R. A. 1949. The opening of milk bottles by birds. British Birds, 42, 347–357Google Scholar
Flinn, M. V. 1997. Culture and the evolution of social learning. Evolution and Human Behaviour, 18, 23–67CrossRefGoogle Scholar
Galef, B. G. Jr. 1992. The question of animal culture. Human Nature, 3, 157–178CrossRefGoogle ScholarPubMed
Gibson, K. R. 1999. Social transmission of facts and skills in the human species: neural mechanisms. In Mammalian Social Learning: Comparative and Ecological Perspectives, ed. H. O. Box, and K. R. Gibson, pp. 351–366. Cambridge: Cambridge University Press
Giraldeau, L.-A., Caraco, T., and Valone, T. J. 1994. Social foraging: individual learning and cultural transmission of innovations. Behavioural Ecology, 5, 35–43CrossRefGoogle Scholar
Gittleman, J. L. 1986. Carnivore brain size, behavioural ecology, and phylogeny. Journal of Mammology, 67, 23–36CrossRefGoogle Scholar
Harvey, P. H. and Krebs, J. R. 1990. Comparing brains. Science, 249, 140–146CrossRefGoogle ScholarPubMed
Harvey, P. H., and Pagel, M. D. 1991. The Comparative Method in Evolutionary Biology. Oxford: Oxford University Press
Harvey, P. H. and Purvis, A. 1991. Comparative methods for explaining adaptations. Nature, 351, 619–624CrossRefGoogle ScholarPubMed
Harvey, P. H. and Rambaut, A. 2000. Comparative analyses for adaptive radiations. Philosophical Transactions of the Royal Society of London, Series B, 355, 1599–1605CrossRefGoogle ScholarPubMed
Harvey, P. H., Martin, R. D., and Clutton-Brock, T. H. 1987. Life histories in comparative perspective. In Primate Societies, ed. B. B. Smuts, D. L. Cheney, R. M. Seyfarth, R. W. Wrangham, and T. T. Struhsaker, pp. 181–196. Chicago, IL: University of Chicago Press
Heyes, C. M. 1994. Social learning in animals: categories and mechanisms. Biological Reviews, 69, 207–231CrossRefGoogle ScholarPubMed
Hinde, R. A. and Fisher, J. 1951. Further observations on the opening of milk bottles by birds. British Birds, 44, 393–396Google Scholar
Hinton, S. J. and Nolan, G. E. 1980. How learning can guide evolution. Complex Systems, 1, 495–502Google Scholar
Holden, C. and Mace, R. 1997. A phylogenetic analysis of the evolution of lactose digestion. Human Biology, 69, 605–628Google ScholarPubMed
Howell, D. C. 1997. Statistical Methods for Psychology, 4th edn. Belmont: Duxbury
Humphrey, N. K. 1976. The social function of intellect. In Growing Points in Ethology, ed. P. P. G. Bateson and R. A. Hinde, pp. 303–317. Cambridge: Cambridge University Press
Jerison, H. J. 1973. Evolution of the Brain and Intelligence. New York: Academic Press
Johnston, T. D. 1982. The selective costs and benefits of learning: an evolutionary analysis. Advances in the Study of Behaviour, 12, 65–106CrossRefGoogle Scholar
Jolicoeur, P., Pirlot, P., Baron, G., and Stephan, H. 1984. Brain structure and correlation patterns in Insectivora, Chiroptera, and primates. Systematic Zoology, 33, 14–29CrossRefGoogle Scholar
Jolly, A. 1966. Lemur social behavior and primate intelligence. Science, 153, 501–506CrossRefGoogle ScholarPubMed
Jouventin, P., Pasteur, G., and Cambefort, J. P. 1976. Observational learning of baboons and avoidance of mimics: exploratory tests. Evolution, 31, 214–218CrossRefGoogle Scholar
Keverne, E. B., Martel, F. L., and Nevison, C. M. 1996. Primate brain evolution: genetic and functional considerations. Proceedings of the Royal Society of London, Series B, 262, 689–696CrossRefGoogle Scholar
Klopfer, P. H. 1961. Observational learning in birds: the establishment of behavioral modes. Behaviour, 17, 71–80CrossRefGoogle Scholar
Krebs, J. R., Sherry, D. F., Healy, S. D., Perry, H., and Vaccerino, A. L. 1989. Hippocampal specialization of food-storing birds. Proceedings of the National Academy of Sciences, USA, 86, 1388–1392CrossRefGoogle ScholarPubMed
Kummer, H. and Goodall, J. 1985. Conditions of innovative behaviour in primates. Philosophical Transactions of the Royal Society of London, Series B, 308, 203–214CrossRefGoogle Scholar
Laland, K. N. 1992. A theoretical investigation of the role of social transmission in evolution. Ethology and Sociobiology, 13, 87–113CrossRefGoogle Scholar
Laland, K. N. and Plotkin, H. C. 1992. Further experimental analysis of the social learning and transmission of foraging information amongst Norway rats. Behavioural Processes, 27, 53–64CrossRefGoogle ScholarPubMed
Lee, P. 1991. Adaptations to environmental change: an evolutionary perspective. In Primate Responses to Environmental Change, ed. H. O. Box, pp. 39–56. London: Chapman & Hall
Lefebvre, L. 1995. The opening of milk-bottles by birds: evidence for accelerating learning rates, but against the wave-of-advance model of cultural transmission. Behavioural Processes, 34, 43–53CrossRefGoogle ScholarPubMed
Lefebvre, L. and Giraldeau, L.-A. 1996. Is social learning an adaptive specialization? In Social Learning in Animals: The Roots of Culture, ed. C. M. Heyes and B. G. Galef Jr., pp. 107–128. London: Academic Press
Lefebvre, L., Palameta, B., and Hatch, K. K. 1996. Is group-living associated with social learning? A comparative test of a gregarious and a territorial columbid. Behaviour, 133, 1–21CrossRefGoogle Scholar
Lefebvre, L., Whittle, P., Lascaris, E., and Finkelstein, A. 1997. Feeding innovations and forebrain size in birds. Animal Behaviour, 53, 549–560CrossRefGoogle Scholar
Lefebvre, L., Nicolakakis, N., and Boire, D. 2002. Tools and Brains in Birds. Behaviour, 139, 939–973CrossRefGoogle Scholar
Macphail, E. M. 1982. Brain and Intelligence in Vertebrates. Oxford: Clarendon Press
Martin, R. D. 1990. Primate Origins and Evolution: A Phylogenetic Reconstruction. London: Chapman & Hall
Martin, P. R. and Bateson, P. 1986. Measuring Behaviour: An Introductory Guide. Cambridge: Cambridge University Press
Martins, E. P. 1993. Comparative studies, phylogenies and predictions of coevolutionary relationships. Behavioral and Brain Sciences, 16, 714–716CrossRefGoogle Scholar
Milton, K. 1988. Foraging behaviour and the evolution of primate intelligence. In Machiavellian Intelligence: Social Expertise and the Evolution of Intellect in Monkeys, Apes and Humans, ed. R. W. Byrne, and A. Whiten, pp. 271–284. Oxford: Oxford University Press
Pagel, M. 1999. Inferring the historical patterns of biological evolution. Nature, 401, 877–884CrossRefGoogle ScholarPubMed
Parker, S. T. and Gibson, K. R. 1977. Object manipulation, tool use and sensorimotor intelligence as feeding adaptations in Cebus monkeys and great apes. Journal of Human Evolution, 6, 623–641CrossRefGoogle Scholar
Passingham, R. E. 1982. The Human Primate. Oxford: W. H. Freeman
Plotkin, H. C. 1994. Darwin Machines and the Nature of Knowledge. London: Penguin
Purvis, A. 1992. Comparative Methods: Theory and Practice. DPhil Thesis, University of Oxford
Purvis, A. 1995. A composite estimate of primate phylogeny. Philosophical Transactions of the Royal Society of London, Series B, 348, 405–421CrossRefGoogle ScholarPubMed
Purvis, A. and Rambaut, A. 1995. Comparative analysis by independent contrasts (CAIC): an Apple Macintosh application for analysing comparative data. Computer Applications in the Biosciences, 11, 247–251Google ScholarPubMed
Purvis, A. and Webster, A. J. 1999. Phylogentically independent comparisons and primate phylogeny. In Comparative Primate Socioecology, ed. P. C. Lee, pp. 44–70. Cambridge: Cambridge University Press
Purvis, A., Gittleman, J. L., and Luh, H.-K. 1994. Truth or consequences: effects of phylogenetic accuracy on two comparative methods. Journal of Theoretical Biology, 167, 293–300CrossRefGoogle Scholar
Reader, S. M. and Laland, K. N. 2001. Primate innovation: sex, age and social rank differences. International Journal of Primatology, 22, 787–805CrossRefGoogle Scholar
Reader, S. M. and Laland, K. N. 2002. Social intelligence, innovation and enhanced brain size in primates. Proceedings of the National Academy of Sciences, USA, 99, 4436–4441CrossRefGoogle ScholarPubMed
Reader, S. M. and Lefebvre, L. 2001. Social learning and sociality. Behavioral and Brain Sciences, 24, 353–355CrossRefGoogle Scholar
Rensch, B. 1956. Increase of learning capability with increase of brain size. American Naturalist, 90, 81–95CrossRefGoogle Scholar
Rensch, B. 1957. The intelligence of elephants. Scientific American, 196, 44–49CrossRefGoogle Scholar
Richerson, P. J. and Boyd, R. 2000. Climate, culture and the evolution of cognition. In The Evolution of Cognition, ed. C. Heyes, and L. Huber, pp. 329–346. Cambridge, MA: MIT Press
Riddell, W. I. 1979. Cerebral indices and behavioral differences. In Development and Evolution of Brain Size: Behavioral Implications, ed. M. E. Hahn, C. Jenson, and B. C. Dudek, pp. 89–109. New York: Academic Press
Rogers, A. R. 1988. Does biology constrain culture?American Anthropologist, 90, 819–831CrossRefGoogle Scholar
Roper, T. J. 1986. Cultural evolution of feeding behaviour in animals. Science Progress, 70, 571–583Google ScholarPubMed
Rowe, N. 1996. The Pictorial Guide to the Living Primates. New York: Pogonias Press
Sasvàri, L. 1979. Observational learning in great, blue and marsh tits. Animal Behaviour, 27, 767–771CrossRefGoogle Scholar
Sasvàri, L. 1985. Different observational learning capacity in juvenile and adult individuals of congeneric bird species. Zietschrift für Tierpsychologie, 69, 293–304CrossRefGoogle Scholar
Sawaguchi, T. 1997. Possible involvement of sexual selection in neocortical evolution of monkeys and apes. Folia Primatologica, 65, 95–99CrossRefGoogle Scholar
Sawaguchi, T. and Kudo, H. 1990. Neocortical development and social structure in primates. Primates, 31, 283–290CrossRefGoogle Scholar
Schlichting, C. D. and Pigliucci, M. 1998. Phenotypic Evolution: A Reaction Norm Perspective. Sunderland, MA: Sinauer
Sherry, D. F. and Galef, B. G. Jr. 1984. Cultural transmission without imitation: milk bottle opening by birds. Animal Behaviour, 32, 937–938CrossRefGoogle Scholar
Sherry, D. and Galef, B. G. Jr. 1990. Social learning without imitation: more about milk bottle opening by birds. Animal Behaviour, 40, 987–989CrossRefGoogle Scholar
Shettleworth, S. J. 1998. Cognition, Evolution, and Behaviour. Oxford: Oxford University Press
Smuts, B. B., Cheney, D. L., Seyfarth, R. M., Wrangham, R. W., and Struhsaker, T. T. (ed.) 1987. Primate Societies. Chicago, IL: University of Chicago Press
Sol, D. and Lefebvre, L. 2000. Forebrain size and foraging innovations predict invasion success in birds introduced to New Zealand. Oikos, 90, 599–605CrossRefGoogle Scholar
Sol, D., Lefebvre, L., and Timmermans, S. 2002. Behavioural flexibility and invasion success in birds. Animal Behaviour, 63, 495–502CrossRefGoogle Scholar
Stephan, H., Frahm, H., and Baron, G. 1981. New and revised data on volumes of brain structure in insectivores and primates. Folia Primatologica, 35, 1–29CrossRefGoogle ScholarPubMed
Timmermans, S., Lefebvre, L., Boire, D., and Basu, P. 2000. Relative size of the hyperstriatum ventrale is the best predictor of feeding innovation rate in birds. Brain, Behavior and Evolution, 56, 196–203CrossRefGoogle ScholarPubMed
Tooby, J. and Cosmides, L. 1989. Evolutionary psychology and the generation of culture, part I. Ethology and Sociobiology, 10, 29–49CrossRefGoogle Scholar
Lawick-Goodall, J. 1970. Tool-using in primates and other vertebrates. Advances in the Study of Behaviour, 3, 95–249Google Scholar
Schaik, C. P., Deaner, R. O., and Merrill, M. Y. 1999. The conditions for tool use in primates: implications for the evolution of material culture. Journal of Human Evolution, 36, 719–741CrossRefGoogle ScholarPubMed
Whiten, A. and Byrne, R. 1988. Taking (Machiavellian) intelligence apart: editorial. In Machiavellian Intelligence: Social Expertise and the Evolution of Intellect in Monkeys, Apes and Humans, ed. R. W. Byrne, and A. Whiten, pp. 50–65. Oxford: Oxford University Press
Whiten, A. and Byrne, R. W. 1997. Machiavellian Intelligence II: Extensions and Evaluations. Cambridge: Cambridge University Press
Wilson, A. C. 1985. The molecular basis of evolution. Scientific American, 253, 148–157CrossRefGoogle Scholar
Wilson, A. C. 1991. From molecular evolution to body and brain evolution. In Perspectives on Cellular Regulation: From Bacteria to Cancer, ed. J. Campisi, D. Cunningham, M. Inouye, and M. Riley, pp. 331–340. New York: Wiley-Liss
Wyles, J. S., Kunkel, J. G., and Wilson, A. C. 1983. Birds, behaviour, and anatomical evolution. Proceedings of the National Academy of Sciences, USA, 80, 4394–4397CrossRefGoogle ScholarPubMed
Wynn, T. 1988. Tools and the evolution of human intelligence. In Machiavellian Intelligence, ed. R. W. Byrne, and A. Whiten, pp. 271–284. Oxford: Oxford University Press
Zilles, K. and Rehkamper, G. 1988. The brain, with special reference to the telencephalon. In Orang-Utan Biology, ed. J. H. Schwartz, pp. 157–176. Oxford: Oxford University Press

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