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Articles
Social learning and the development of individual and group behaviour in mammal societies
Published:12 April 2011https://doi.org/10.1098/rstb.2010.0312
Abstract
As in human societies, social learning may play an important role in shaping individual and group characteristics in other mammals. Here, we review research on non-primate mammals, concentrating on work at our long-term meerkat study site, where longitudinal data and field experiments have generated important insights into the role of social learning under natural conditions. Meerkats live under high predation pressure and occupy a difficult foraging niche. Accordingly, pups make extensive use of social information in learning to avoid predation and obtain food. Where individual learning is costly or opportunities are lacking, as in the acquisition of prey-handling skills, adults play an active role in promoting learning through teaching. Social learning can also cause information to spread through groups, but our data suggest that this does not necessarily result in homogeneous, group-wide traditions. Moreover, traditions are commonly eroded by individual learning. We suggest that traditions will only persist where there are high costs of deviating from the group norm or where skill development requires extensive time and effort. Persistent traditions could, theoretically, modify selection pressures and influence genetic evolution. Further empirical studies of social learning in natural populations are now urgently needed to substantiate theoretical claims.
References
- 1
Richerson P. J.& Boyd R. . 2005 Not by genes alone: how culture transformed human evolution. Chicago, IL: University of Chicago Press. Google Scholar - 2
Boyd R.& Richerson P. . 1985 Culture and the evolutionary process. Chicago, IL: University of Chicago Press. Google Scholar - 3
Danchin E., Giraldeau L. A., Valone T. J.& Wagner R. H. . 2004 Public information: from nosy neighbors to cultural evolution. Science 305, 487–491.doi:10.1126/science.1098254 (doi:10.1126/science.1098254). Crossref, PubMed, Web of Science, Google Scholar - 4
Laland K. N., Odling-Smee J.& Feldman M. W. . 2000 Niche construction, biological evolution, and cultural change. Behav. Brain Sci. 23, 131–175.doi:10.1017/S0140525X00002417 (doi:10.1017/S0140525X00002417). Crossref, PubMed, Web of Science, Google Scholar - 5
Heyes C. M.& Galef B. G. . 1996 Social learning in animals: the roots of culture. San Diego, CA: Academic Press. Google Scholar - 6
Laland K. N., Kendal J. R.& Kendal R. L. . 2009 Animal culture: problems and solutions. The question of animal culture (eds, Laland K. N.& Galef B. G. ), pp. 174–197. Cambridge, MA: Harvard University Press. Crossref, Google Scholar - 7
Whiten A., Hinde R. A., Laland K. N.& Stringer C. B. . 2011 Culture evolves. Phil. Trans. R. Soc. B 366, 938–948.doi:10.1098/rstb.2010.0372 (doi:10.1098/rstb.2010.0372). Link, Web of Science, Google Scholar - 8
Whiten A.& Mesoudi A. . 2008 Establishing an experimental science of culture: animal social diffusion experiments. Phil. Trans. R. Soc. B 363, 3477–3488.doi:10.1098/rstb.2008.0134 (doi:10.1098/rstb.2008.0134). Link, Web of Science, Google Scholar - 9
Laland K. N.& Janik V. M. . 2006 The animal cultures debate. Trends Ecol. Evol. 21, 542–547.doi:10.1016/j.tree.2006.06.005 (doi:10.1016/j.tree.2006.06.005). Crossref, PubMed, Web of Science, Google Scholar - 10
Perry S. . 2011 Social traditions and social learning in capuchin monkeys (Cebus). Phil. Trans. R. Soc. B 366, 988–996.doi:10.1098/rstb.2010.0317 (doi:10.1098/rstb.2010.0317). Link, Web of Science, Google Scholar - 11
Whiten A. . 2011 The scope of culture in chimpanzees, humans and ancestral apes. Phil. Trans. R. Soc. B 366, 997–1007.doi:10.1098/rstb.2010.0334 (doi:10.1098/rstb.2010.0334). Link, Web of Science, Google Scholar - 12
Slagsvold T.& Wiebe K. L. . 2011 Social learning in birds and its role in shaping a foraging niche. Phil. Trans. R. Soc. B. 366, 969–977.doi:10.1098/rstb.2010.0343 (doi:10.1098/rstb.2010.0343). Link, Web of Science, Google Scholar - 13
Laland K. N., Atton N.& Webster M. M. . 2011 From fish to fashion: experimental and theoretical insights into the evolution of culture. Phil. Trans. R. Soc. B 366, 958–968.doi:10.1098/rstb.2010.0328 (doi:10.1098/rstb.2010.0328). Link, Web of Science, Google Scholar - 14
Laland K. N.& Kendal J. R. . 2003 What the models say about social learning. The biology of traditions: models and evidence (eds, Fragaszy D. M.& Perry S. ), pp. 33–55. Cambridge, UK: Cambridge University Press. Crossref, Google Scholar - 15
Griffin A. S. . 2004 Social learning about predators: a review and prospectus. Learn. Behav. 32, 131–140. Crossref, PubMed, Web of Science, Google Scholar - 16
Davies N. B.& Welbergen J. A. . 2009 Social transmission of a host defense against cuckoo parasitism. Science 324, 1318–1320.doi:10.1126/science.1172227 (doi:10.1126/science.1172227). Crossref, PubMed, Web of Science, Google Scholar - 17
Reader S. M., Kendal J. R.& Laland K. N. . 2003 Social learning of foraging sites and escape routes in wild Trinidadian guppies. Anim. Behav. 66, 729–739.doi:10.1006/anbe.2003.2252 (doi:10.1006/anbe.2003.2252). Crossref, Web of Science, Google Scholar - 18
Graw B.& Manser M. B. . 2007 The function of mobbing in cooperative meerkats. Anim. Behav. 74, 507–517.doi:10.1016/j.anbehav.2006.11.021 (doi:10.1016/j.anbehav.2006.11.021). Crossref, Web of Science, Google Scholar - 19
Manser M. B., Seyfarth R. M.& Cheney D. L. . 2002 Suricate alarm calls signal predator class and urgency. Trends Cogn. Sci. 6, 55–57.doi:10.1016/S1364-6613(00)01840-4 (doi:10.1016/S1364-6613(00)01840-4). Crossref, PubMed, Web of Science, Google Scholar - 20
Hollén L. I.& Manser M. B. . 2006 Ontogeny of alarm call responses in meerkats, Suricata suricatta: the roles of age, sex and nearby conspecifics. Anim. Behav. 72, 1345–1353.doi:10.1016/j.anbehav.2006.03.020 (doi:10.1016/j.anbehav.2006.03.020). Crossref, Web of Science, Google Scholar - 21
Lonsdorf E. V., Eberly L. E.& Pusey A. E. . 2004 Sex differences in learning in chimpanzees. Nature 428, 715–716.doi:10.1038/428715a (doi:10.1038/428715a). Crossref, PubMed, Web of Science, Google Scholar - 22
Cheney D.& Seyfarth R. . 1990 How monkeys see the world: inside the mind of another species. Chicago, IL: University of Chicago Press. Crossref, Google Scholar - 23
Hollén L. I., Clutton-Brock T.& Manser M. B. . 2008 Ontogenetic changes in alarm-call production and usage in meerkats (Suricata suricatta): adaptations or constraints? Behav. Ecol. Sociobiol. 62, 821–829.doi:10.1007/s00265-007-0508-x (doi:10.1007/s00265-007-0508-x). Crossref, Web of Science, Google Scholar - 24
Mateo J. M.& Holmes W. G. . 1997 Development of alarm-call responses in Belding's ground squirrels: the role of dams. Anim. Behav. 54, 509–524.doi:10.1006/anbe.1996.0446 (doi:10.1006/anbe.1996.0446). Crossref, PubMed, Web of Science, Google Scholar - 25
Mineka S.& Cook M. . 1988 Social learning and the acquisition of snake fear in monkeys. Social learning: psychological and biological perspectives (eds, Zentall T. R.& Galef B. G. ), pp. 51–73. Hillsdale, NJ: Erlbaum. Google Scholar - 26
Davies N. B., Madden J. R.& Butchart S. H. M. . 2004 Learning fine-tunes a specific response of nestlings to the parental alarm calls of their own species. Proc. R. Soc. Lond. B 271, 2297–2304.doi:10.1098/rspb.2004.2835 (doi:10.1098/rspb.2004.2835). Link, Web of Science, Google Scholar - 27
Heinsohn R. G. . 1991 Slow learning of foraging skills and extended parental care in cooperatively breeding white-winged choughs. Am. Nat. 137, 864–881.doi:10.1086/285198 (doi:10.1086/285198). Crossref, Web of Science, Google Scholar - 28
Thornton A.& Hodge S. J. . 2009 The development of foraging microhabitat preferences in meerkats. Behav. Ecol. 20, 103–110.doi:10.1093/beheco/arn120 (doi:10.1093/beheco/arn120). Crossref, Web of Science, Google Scholar - 29
Giraldeau L. A. . 1984 Group foraging: the skill pool effect and frequency-dependent learning. Am. Nat. 124, 72–79.doi:10.1086/284252 (doi:10.1086/284252). Crossref, Web of Science, Google Scholar - 30
Galef B. G.& Giraldeau L. A. . 2001 Social influences on foraging in vertebrates: causal mechanisms and adaptive functions. Anim. Behav. 61, 3–15.doi:10.1006/anbe.2000.1557 (doi:10.1006/anbe.2000.1557). Crossref, PubMed, Web of Science, Google Scholar - 31
Galef B. G. . 2003 ‘Traditional’ foraging behaviors of brown and black rats (Rattus norvegicus and Rattus rattus). The biology of traditions: models and evidence (eds, Fragaszy D. M.& Perry S. ), pp. 159–186. Cambridge, UK: Cambridge University Press. Crossref, Google Scholar - 32
Hepper P. G. . 1988 Adaptive fetal learning: prenatal exposure to garlic affects postnatal preferences. Anim. Behav. 36, 935–936.doi:10.1016/S0003-3472(88)80177-5 (doi:10.1016/S0003-3472(88)80177-5). Crossref, Web of Science, Google Scholar - 33
Galef B. G.& Sherry D. F. . 1973 Mothers milk: a medium for transmission of cues reflecting flavor of mother's diet. J. Comp. Physiol. Psychol. 83, 374–378.doi:10.1037/h0034665 (doi:10.1037/h0034665). Crossref, PubMed, Web of Science, Google Scholar - 34
Galef B. G.& Stein M. . 1985 Demonstrator influence on observer diet preference: analyses of critical social interactions and olfactory signals. Anim. Learn. Behav. 13, 31–38. Crossref, Google Scholar - 35
Valsecchi P.& Galef B. G. . 1989 Social influences on the food preferences of house mice (Mus musculus). Int. J. Comp. Psychol. 2, 245–256. Crossref, Google Scholar - 36
Lupfer-Johnson G.& Ross J. . 2007 Dogs acquire food preferences from interacting with recently fed conspecifics. Behav. Processes 74, 104–106.doi:10.1016/j.beproc.2006.09.006 (doi:10.1016/j.beproc.2006.09.006). Crossref, PubMed, Web of Science, Google Scholar - 37
Box H. O.& Gibson K. R. (eds) 1999 Mammalian social learning: comparative and ecological perspectives. Cambridge, UK: Cambridge University Press. Google Scholar - 38
Thornton A. . 2008 Social learning about novel foods by young meerkats. Anim. Behav. 76, 1411–1421.doi:10.1016/j.anbehav.2008.07.007 (doi:10.1016/j.anbehav.2008.07.007). Crossref, Web of Science, Google Scholar - 39
Thornton A.& Raihani N. J. . 2008 The evolution of teaching. Anim. Behav. 75, 1823–1836.doi:10.1016/j.anbehav.2007.12.014 (doi:10.1016/j.anbehav.2007.12.014). Crossref, Web of Science, Google Scholar - 40
Sargeant B. L.& Mann J. . 2009 Developmental evidence for foraging traditions in wild bottlenose dolphins. Anim. Behav. 78, 715–721.doi:10.1016/j.anbehav.2009.05.037 (doi:10.1016/j.anbehav.2009.05.037). Crossref, Web of Science, Google Scholar - 41
Terkel J. . 1996 Cultural transmission of feeding behavior in the black rat (Rattus rattus). Social learning in animals: the roots of culture (eds, Heyes C. M.& Galef B. G. Jr), pp. 17–47. San Diego, CA: Academic Press. Crossref, Google Scholar - 42
Premack D.& Premack A. J. . 1996 Why animals lack pedagogy and some cultures have more of it than others. Handbook of education and human development: new models of learning, teaching and schooling (eds, Olson D. R.& Torrance N. ), pp. 302–323. Oxford, UK: Blackwell. Google Scholar - 43
Strauss S., Ziv M.& Stein A. . 2002 Teaching as a natural cognition and its relations to preschoolers' developing theory of mind. Cogn. Dev. 17, 1473–1487.doi:10.1016/S0885-2014(02)00128-4 (doi:10.1016/S0885-2014(02)00128-4). Crossref, Web of Science, Google Scholar - 44
Tomasello M., Kruger A. C.& Ratner H. H. . 1993 Cultural learning. Behav. Brain Sci. 16, 495–552.doi:10.1017/S0140525X0003123X (doi:10.1017/S0140525X0003123X). Crossref, Web of Science, Google Scholar - 45
Caro T. M.& Hauser M. D. . 1992 Is there teaching in nonhuman animals? Q. Rev. Biol. 67, 151–174.doi:10.1086/417553 (doi:10.1086/417553). Crossref, PubMed, Web of Science, Google Scholar - 46
Caro T. M. . 1980 The effects of experience on the predatory patterns of cats. Behav. Neural Biol. 29, 1–28.doi:10.1016/S0163-1047(80)92442-5 (doi:10.1016/S0163-1047(80)92442-5). Crossref, PubMed, Google Scholar - 47
Thornton A.& McAuliffe K. . 2006 Teaching in wild meerkats. Science 313, 227–229.doi:10.1126/science.1128727 (doi:10.1126/science.1128727). Crossref, PubMed, Web of Science, Google Scholar - 48
Raihani N. J.& Ridley A. R. . 2008 Experimental evidence for teaching in wild pied babblers. Anim. Behav. 75, 3–11.doi:10.1016/j.anbehav.2007.07.024 (doi:10.1016/j.anbehav.2007.07.024). Crossref, Web of Science, Google Scholar - 49
Franks N. R.& Richardson T. . 2006 Teaching in tandem-running ants. Nature 439, 153.doi:10.1038/439153a (doi:10.1038/439153a). Crossref, PubMed, Web of Science, Google Scholar - 50
McComb K.& Clutton-Brock T. . 1994 Is mate choice copying or aggregation responsible for skewed distributions of females on leks? Proc. R. Soc. Lond. B 255, 13–19.doi:10.1098/rspb.1994.0003 (doi:10.1098/rspb.1994.0003). Link, Web of Science, Google Scholar - 51
Godin J. G. J., Herdman E. J. E.& Dugatkin L. A. . 2005 Social influences on female mate choice in the guppy, Poecilia reticulata: generalized and repeatable trait-copying behaviour. Anim. Behav. 69, 999–1005.doi:10.1016/j.anbehav.2004.07.016 (doi:10.1016/j.anbehav.2004.07.016). Crossref, Web of Science, Google Scholar - 52
White D. J.& Galef B. G. . 2000 ‘Culture’ in quail: social influences on mate choices of female Coturnix japonica. Anim. Behav. 59, 975–979.doi:10.1006/anbe.1999.1402 (doi:10.1006/anbe.1999.1402). Crossref, PubMed, Web of Science, Google Scholar - 53
Janik V. M.& Slater P. J. B. . 2000 The different roles of social learning in vocal communication. Anim. Behav. 60, 1–11.doi:10.1006/anbe.2000.1410 (doi:10.1006/anbe.2000.1410). Crossref, PubMed, Web of Science, Google Scholar - 54
Beltman J. B., Haccou P.& Ten Cate C. . 2004 Learning and colonization of new niches: a first step toward speciation. Evolution 58, 35–46. Crossref, PubMed, Web of Science, Google Scholar - 55
Laland K. N. . 1994 On the evolutionary consequences of sexual imprinting. Evolution 48, 477–489.doi:10.2307/2410106 (doi:10.2307/2410106). Crossref, PubMed, Web of Science, Google Scholar - 56
Clutton-Brock T.& McAuliffe K. . 2009 Female mate choice in mammals. Q. Rev. Biol. 84, 3–27.doi:10.1086/596461 (doi:10.1086/596461). Crossref, PubMed, Web of Science, Google Scholar - 57
Davidson S. M.& Wilkinson G. S. . 2004 Function of male song in the greater white-lined bat, Saccopteryx bilineata. Anim. Behav. 67, 883–891.doi:10.1016/j.anbehav.2003.06.016 (doi:10.1016/j.anbehav.2003.06.016). Crossref, Web of Science, Google Scholar - 58
Rendell L.& Whitehead H. . 2001 Culture in whales and dolphins. Behav. Brain Sci. 24, 309–324. Crossref, PubMed, Web of Science, Google Scholar - 59
Fragaszy D. M.& Perry S. . 2003 Towards a biology of traditions. The biology of traditions: models and evidence (eds, Fragaszy D. M.& Perry S. ), pp. 1–32. Cambridge, UK: Cambridge University Press. Crossref, Google Scholar - 60
McGrew W. C. . 2009 Ten dispatches from the chimpanzee culture wars, plus postcript (revisiting the battlefronts). The question of animal culture (eds, Laland K. N.& Galef B. G. ). Cambridge, MA: Harvard University Press. Google Scholar - 61
Laland K. N.& Hoppitt W. . 2003 Do animals have culture? Evol. Anthropol. 12, 150–159.doi:10.1002/evan.10111 (doi:10.1002/evan.10111). Crossref, Web of Science, Google Scholar - 62
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 (doi:10.1098/rstb.2006.1998). Link, Web of Science, Google Scholar - 63
Perry S. . 2009 Are nonhuman primates likely to exhibit cultural capacities like those of humans? In The question of animal culture (eds, Laland K. N.& Galef B. G. ). Cambridge, MA: Harvard University Press. Google Scholar - 64
Tomasello M. . 1994 The question of chimpanzee culture. Chimpanzee cultures (eds, Wrangham R., McGrew W., de Waal F.& Heltne P. ), pp. 301–317. Cambridge, MA: Harvard University Press. Google Scholar - 65
Kendal R. L., Kendal J. R., Hoppitt W.& Laland K. N. . 2009 Identifying social learning in animal populations: a new ‘option-bias' method. PLoS ONE 4, e6541.doi:10.1371/journal.pone.0006541 (doi:10.1371/journal.pone.0006541). Crossref, PubMed, Web of Science, Google Scholar - 66
Müller C. A.& Cant M. A. . 2010 Imitation and traditions in wild banded mongooses. Curr. Biol. 20, 1171–1175.doi:10.1016/j.cub.2010.04.037 (doi:10.1016/j.cub.2010.04.037). Crossref, PubMed, Web of Science, Google Scholar - 67
Sargeant B. L.& Mann J. . 2009 From social learning to culture: intrapopulation variation in bottlenose dolphins. The question of animal culture (eds, Laland K. N.& Galef B. G. ). Cambridge, MA: Harvard University Press. Google Scholar - 68
Thornton A.& Malapert A. . 2009 Experimental evidence for social transmission of food acquisition techniques in wild meerkats. Anim. Behav. 78, 255–264.doi:10.1016/j.anbehav.2009.04.021 (doi:10.1016/j.anbehav.2009.04.021). Crossref, Web of Science, Google Scholar - 69
Helfman G. S.& Schultz E. T. . 1984 Social transmission of behavioral traditions in a coral reef fish. Anim. Behav. 32, 379–384.doi:10.1016/S0003-3472(84)80272-9 (doi:10.1016/S0003-3472(84)80272-9). Crossref, Web of Science, Google Scholar - 70
Warner R. R. . 1988 Traditionality of mating site preferences in a coral reef fish. Nature 335, 719–721.doi:10.1038/335719a0 (doi:10.1038/335719a0). Crossref, Web of Science, Google Scholar - 71
van de Waal E., Renevey N., Favre C. M.& Bshary R. . 2010 Selective attention to philopatric models causes directed social learning in wild vervet monkeys. Proc. R. Soc. B 277, 2105–2111.doi:10.1098/rspb.2009.2260 (doi:10.1098/rspb.2009.2260). Link, Web of Science, Google Scholar - 72
Claidière N.& Sperber D. . 2010 Imitation explains the propagation, not the stability of animal culture. Proc. R. Soc. B 277, 651–659.doi:10.1098/rspb.2009.1615 (doi:10.1098/rspb.2009.1615). Link, Web of Science, Google Scholar - 73
Galef B. G.& Allen C. . 1995 A new model system for studying behavioral traditions in animals. Anim. Behav. 50, 705–717.doi:10.1016/0003-3472(95)80131-6 (doi:10.1016/0003-3472(95)80131-6). Crossref, Web of Science, Google Scholar - 74
Giraldeau L. A.& Lefebvre L. . 1987 Scrounging prevents cultural transmission of food-finding behavior in pigeons. Anim. Behav. 35, 387–394.doi:10.1016/S0003-3472(87)80262-2 (doi:10.1016/S0003-3472(87)80262-2). Crossref, Web of Science, Google Scholar - 75
Rieucau G.& Giraldeau L.-A. . 2011 Exploring the costs and benefits of social information use: an appraisal of current experimental evidence. Phil. Trans. R. Soc. B 366, 949–957.doi:10.1098/rstb.2010.0325 (doi:10.1098/rstb.2010.0325). Link, Web of Science, Google Scholar - 76
Thornton A.& Malapert A. . 2009 The rise and fall of an arbitrary tradition: an experiment with wild meerkats. Proc. R. Soc. B 276, 1269–1276.doi:10.1098/rspb.2008.1794 (doi:10.1098/rspb.2008.1794). Link, Web of Science, Google Scholar - 77
Henrich J., 2010 Markets, religion, community size, and the evolution of fairness and punishment. Science 327, 1480–1484.doi:10.1126/science.1182238 (doi:10.1126/science.1182238). Crossref, PubMed, Web of Science, Google Scholar - 78
Thornton A., Samson J.& Clutton-Brock T. . 2010 Multi-generational persistence of traditions in neighbouring meerkat groups. Proc. R. Soc. B 277, 3623–3629.doi:10.1098/rspb.2010.0611 (doi:10.1098/rspb.2010.0611). Link, Web of Science, Google Scholar - 79
Laland K. N., Odling-Smee J.& Myles S. . 2010 How culture shaped the human genome: bringing genetics and the human sciences together. Nat. Rev. Genet. 11, 137–148.doi:10.1038/nrg2734 (doi:10.1038/nrg2734). Crossref, PubMed, Web of Science, Google Scholar - 80
Durham W. H. . 1991 Coevolution: genes, culture, and human diversity. Stanford, CA: Stanford University Press. Google Scholar - 81
Mesoudi A., Whiten A.& Laland K. N. . 2006 Towards a unified science of cultural evolution. Behav. Brain Sci. 29, 329–383. Crossref, PubMed, Web of Science, Google Scholar - 82
Boesch C. . 1993 Towards a new image of culture in wild chimpanzees. Behav. Brain Sci. 16, 514–515.doi:10.1017/S0140525X00031277 (doi:10.1017/S0140525X00031277). Crossref, Web of Science, Google Scholar - 83
Hunt G. R.& Gray R. D. . 2003 Diversification and cumulative evolution in New Caledonian crow tool manufacture. Proc. R. Soc. Lond. B 270, 867–874.doi:10.1098/rspb.2002.2302 (doi:10.1098/rspb.2002.2302). Link, Web of Science, Google Scholar - 84
Kendal J. R., Rendell L., Pike T. W.& Laland K. N. . 2009 Nine-spined sticklebacks deploy a hill-climbing social learning strategy. Behav. Ecol. 20, 238–244.doi:10.1093/beheco/arp016 (doi:10.1093/beheco/arp016). Crossref, Web of Science, Google Scholar - 85
Galef B. G. . 1992 The question of animal culture. Hum. Nat. 3, 157–178.doi:10.1007/BF02692251 (doi:10.1007/BF02692251). Crossref, PubMed, Google Scholar - 86
Huber L., Range F., Voelkl B., Szucsich A., Viranyi Z.& Miklosi A. . 2009 The evolution of imitation: what do the capacities of non-human animals tell us about the mechanisms of imitation? Phil. Trans. R. Soc. B 364, 2299–2309.doi:10.1098/rstb.2009.0060 (doi:10.1098/rstb.2009.0060). Link, Web of Science, Google Scholar - 87
Caldwell C. A.& Millen A. E. . 2009 Social learning mechanisms and cumulative cultural evolution: is imitation necessary? Psychol. Sci. 20, 1478–1483.doi:10.1111/j.1467-9280.2009.02469.x (doi:10.1111/j.1467-9280.2009.02469.x). Crossref, PubMed, Web of Science, Google Scholar - 88
Csibra G.& Gergely G. . 2011 Natural pedagogy as evolutionary adaptation. Phil. Trans. R. Soc. B 366, 1149–1157.doi:10.1098/rstb.2010.0319 (doi:10.1098/rstb.2010.0319). Link, Web of Science, Google Scholar - 89
Lyons D. E., Damrosch D. H., Lin J. K., Macris D. M.& Keil F. C. . 2011 The scope and limits of overimitation in the transmission of artefact culture. Phil. Trans. R. Soc. B 366, 1158–1167.doi:10.1098/rstb.2010.0335 (doi:10.1098/rstb.2010.0335). Link, Web of Science, Google Scholar - 90
Thornton A.& Raihani N. J. . 2010 Identifying teaching in wild animals. Learn. Behav. 38, 297–309.doi:10.3758/LB.38.3.297 (doi:10.3758/LB.38.3.297). Crossref, PubMed, Web of Science, Google Scholar - 91
Hrdy S. B. . 2009 Mothers and others: the evolutionary origins of mutual understanding. Cambridge, MA: Harvard University Press. Google Scholar - 92
Tomasello M., Carpenter M., Call J., Behne T.& Moll H. . 2005 Understanding and sharing intentions: the origins of shared cognition. Behav. Brain Sci. 28, 675–735. Crossref, PubMed, Web of Science, Google Scholar - 93
Hewlett B. S., Fouts H. N., Boyette A. H.& Hewlett B. L. . 2011 Social learning among Congo Basin hunter–gatherers. Phil. Trans. R. Soc. B 366, 1168–1178.doi:10.1098/rstb.2010.0373 (doi:10.1098/rstb.2010.0373). Link, Web of Science, Google Scholar - 94
McComb K., Moss C., Durant S. M., Baker L.& Sayialel S. . 2001 Matriarchs as repositories of social knowledge in African elephants. Science 292, 491–494.doi:10.1126/science.1057895 (doi:10.1126/science.1057895). Crossref, PubMed, Web of Science, Google Scholar - 95
Whiten A. . 2005 The second inheritance system of chimpanzees and humans. Nature 437, 52–55.doi:10.1038/nature04023 (doi:10.1038/nature04023). Crossref, PubMed, Web of Science, Google Scholar
