Social learning and the development of individual and group behaviour in mammal societies

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.

[1]  A. Thornton,et al.  Teaching in Wild Meerkats , 2006, Science.

[2]  M. Cant,et al.  Imitation and Traditions in Wild Banded Mongooses , 2010, Current Biology.

[3]  Bernhard Voelkl,et al.  The evolution of imitation: what do the capacities of non-human animals tell us about the mechanisms of imitation? , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[4]  J. Mann,et al.  Developmental evidence for foraging traditions in wild bottlenose dolphins , 2009, Animal Behaviour.

[5]  Nigel R. Franks,et al.  Teaching in tandem-running ants , 2006, Nature.

[6]  M. Tomasello,et al.  Understanding and sharing intentions: The origins of cultural cognition , 2005, Behavioral and Brain Sciences.

[7]  A. Thornton,et al.  Social learning about novel foods in young meerkats , 2008, Animal Behaviour.

[8]  Gwen Lupfer-Johnson,et al.  Dogs acquire food preferences from interacting with recently fed conspecifics , 2007, Behavioural Processes.

[9]  K. Laland,et al.  ON THE EVOLUTIONARY CONSEQUENCES OF SEXUAL IMPRINTING , 1994, Evolution; international journal of organic evolution.

[10]  A. Whiten The scope of culture in chimpanzees, humans and ancestral apes , 2011, Philosophical Transactions of the Royal Society B: Biological Sciences.

[11]  Marta B. Manser,et al.  The function of mobbing in cooperative meerkats , 2007, Animal Behaviour.

[12]  Andrew Whiten,et al.  The evolution of animal ‘cultures’ and social intelligence , 2007, Philosophical Transactions of the Royal Society B: Biological Sciences.

[13]  G. Hunt,et al.  Diversification and cumulative evolution in New Caledonian crow tool manufacture , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[14]  Susan K. Perry,et al.  The Biology of Traditions: Models and Evidence , 2008 .

[15]  T. Caro The effects of experience on the predatory patterns of cats. , 1980, Behavioral and neural biology.

[16]  Dan Sperber,et al.  Imitation explains the propagation, not the stability of animal culture , 2010, Proceedings of the Royal Society B: Biological Sciences.

[17]  S. Mineka,et al.  Social learning and the acquisition of snake fear in monkeys. , 1988 .

[18]  G. Wilkinson,et al.  Function of male song in the greater white-lined bat, Saccopteryx bilineata , 2004, Animal Behaviour.

[19]  David J. White,et al.  ‘Culture’ in quail: social influences on mate choices of female Coturnix japonica , 2000, Animal Behaviour.

[20]  Barry S. Hewlett,et al.  Social learning among Congo Basin hunter–gatherers , 2011, Philosophical Transactions of the Royal Society B: Biological Sciences.

[21]  T. Clutton‐Brock,et al.  Multi-generational persistence of traditions in neighbouring meerkat groups , 2010, Proceedings of the Royal Society B: Biological Sciences.

[22]  C. Boesch Towards a new image of culture in wild chimpanzees? , 1993, Behavioral and Brain Sciences.

[23]  G. Csibra,et al.  Natural pedagogy as evolutionary adaptation , 2011, Philosophical Transactions of the Royal Society B: Biological Sciences.

[24]  Kevin N. Laland,et al.  The Biology of Traditions: What the models say about social learning , 2003 .

[25]  Kevin N Laland,et al.  Culture evolves , 2011, Philosophical Transactions of the Royal Society B: Biological Sciences.

[26]  M. Feldman,et al.  Niche construction, biological evolution, and cultural change , 2000, Behavioral and Brain Sciences.

[27]  Dorothy M. Fragaszy,et al.  Towards a Biology of Traditions , 2003 .

[28]  Christine A Caldwell,et al.  Social Learning Mechanisms and Cumulative Cultural Evolution , 2009, Psychological science.

[29]  G. Helfman,et al.  Social transmission of behavioural traditions in a coral reef fish , 1984, Animal Behaviour.

[30]  Jeremy R. Kendal,et al.  Identifying Social Learning in Animal Populations: A New ‘Option-Bias’ Method , 2009, PloS one.

[31]  T. Valone,et al.  Public Information: From Nosy Neighbors to Cultural Evolution , 2004, Science.

[32]  R. Heinsohn Slow Learning of Foraging Skills and Extended Parental Care in Cooperatively Breeding White-Winged Choughs , 1991, The American Naturalist.

[33]  Alex Mesoudi,et al.  Establishing an experimental science of culture: animal social diffusion experiments , 2008, Philosophical Transactions of the Royal Society B: Biological Sciences.

[34]  Marta B. Manser,et al.  Ontogeny of alarm call responses in meerkats, Suricata suricatta: the roles of age, sex and nearby conspecifics , 2006, Animal Behaviour.

[35]  D. Sherry,et al.  Mother's milk: a medium for transmission of cues reflecting the flavor of mother's diet. , 1973, Journal of comparative and physiological psychology.

[36]  S. Perry Social traditions and social learning in capuchin monkeys (Cebus) , 2011, Philosophical Transactions of the Royal Society B: Biological Sciences.

[37]  T. Clutton‐Brock,et al.  Female Mate Choice in Mammals , 2009, The Quarterly Review of Biology.

[38]  A. Thornton,et al.  The development of foraging microhabitat preferences in meerkats , 2009 .

[39]  Hal Whitehead,et al.  Culture in whales and dolphins , 2001, Behavioral and Brain Sciences.

[40]  B. Galef,et al.  Demonstrator influence on observer diet preference: Analyses of critical social interactions and olfactory signals , 1985 .

[41]  R. Bshary,et al.  Selective attention to philopatric models causes directed social learning in wild vervet monkeys , 2010, Proceedings of the Royal Society B: Biological Sciences.

[42]  P. C. Lee How monkeys see the world: Inside the mind of another species , 1990 .

[43]  C. Heyes,et al.  Social learning in animals : the roots of culture , 1996 .

[44]  L. Giraldeau,et al.  Scrounging prevents cultural transmission of food-finding behaviour in pigeons , 1987, Animal Behaviour.

[45]  André Orléan,et al.  The Evolution of Imitation , 1998 .

[46]  L. Giraldeau,et al.  Group Foraging: The Skill Pool Effect and Frequency-Dependent Learning , 1984, The American Naturalist.

[47]  A. Thornton,et al.  Identifying teaching in wild animals , 2010, Learning & behavior.

[48]  M. Tomasello,et al.  Understanding and sharing intentions , 2005 .

[49]  T. Caro,et al.  Is There Teaching in Nonhuman Animals? , 1992, The Quarterly Review of Biology.

[50]  J. Bruner,et al.  Cultural learning. Author's reply , 1993 .

[51]  S. Strauss,et al.  Teaching as a natural cognition and its relations to preschoolers’ developing theory of mind , 2002 .

[52]  K. Gibson,et al.  Mammalian social learning : comparative and ecological perspectives , 1999 .

[53]  A. Thornton,et al.  The rise and fall of an arbitrary tradition: an experiment with wild meerkats , 2009, Proceedings of the Royal Society B: Biological Sciences.

[54]  Robert M. Seyfarth,et al.  Suricate alarm calls signal predator class and urgency , 2002, Trends in Cognitive Sciences.

[55]  Joseph Terkel,et al.  Cultural Transmission of Feeding Behavior in the Black Rat (Rattus rattus) , 1996 .

[56]  Kevin N. Laland,et al.  Do animals have culture? , 2003 .

[57]  Aurore Malapert,et al.  Experimental evidence for social transmission of food acquisition techniques in wild meerkats , 2009, Animal Behaviour.

[58]  S. Hrdy Mothers and Others: The Evolutionary Origins of Mutual Understanding , 2009 .

[59]  K. Laland,et al.  Towards a unified science of cultural evolution. , 2006, The Behavioral and brain sciences.

[60]  T. Clutton‐Brock,et al.  Is mate choice copying or aggregation responsible for skewed distributions of females on leks? , 1994, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[61]  A. Thornton,et al.  The evolution of teaching , 2008, Animal Behaviour.

[62]  T. Clutton‐Brock,et al.  Ontogenetic changes in alarm-call production and usage in meerkats (Suricata suricatta): adaptations or constraints? , 2008, Behavioral Ecology and Sociobiology.

[63]  L. Giraldeau,et al.  Exploring the costs and benefits of social information use: an appraisal of current experimental evidence , 2011, Philosophical Transactions of the Royal Society B: Biological Sciences.

[64]  B. Galef The question of animal culture , 1992, Human nature.

[65]  J. Henrich,et al.  Markets, Religion, Community Size, and the Evolution of Fairness and Punishment , 2010, Science.

[66]  B. Galef,et al.  A new model system for studying behavioural traditions in animals , 1995, Animal Behaviour.

[67]  Martin H. Levinson Not by Genes Alone: How Culture Transformed Human Evolution , 2006 .

[68]  L. Dugatkin,et al.  Social influences on female mate choice in the guppy, Poecilia reticulata: generalized and repeatable trait-copying behaviour , 2005, Animal Behaviour.

[69]  B. Galef,et al.  Social Influences on the Food Preferences of House Mice (Mus Musculus) , 1989, International Journal of Comparative Psychology.

[70]  N. Raihani,et al.  Experimental evidence for teaching in wild pied babblers , 2008, Animal Behaviour.

[71]  Tore Slagsvold,et al.  Social learning in birds and its role in shaping a foraging niche , 2011, Philosophical Transactions of the Royal Society B: Biological Sciences.

[72]  S. Durant,et al.  Matriarchs As Repositories of Social Knowledge in African Elephants , 2001, Science.

[73]  Mary C. Brennan,et al.  on the , 1982 .

[74]  K. Laland,et al.  How culture shaped the human genome: bringing genetics and the human sciences together , 2010, Nature Reviews Genetics.

[75]  J. Mateo,et al.  Development of alarm-call responses in Belding's ground squirrels: the role of dams , 1997, Animal Behaviour.

[76]  P. Slater,et al.  The different roles of social learning in vocal communication , 2000, Animal Behaviour.

[77]  Andrew Whiten,et al.  The second inheritance system of chimpanzees and humans , 2005, Nature.

[78]  R. Warner,et al.  Traditionality of mating-site preferences in a coral reef fish , 1988, Nature.

[79]  Allon J. Uhlmann Coevolution: genes, culture and human diversity , 1993 .

[80]  L. Eberly,et al.  Sex differences in learning in chimpanzees , 2004, Nature.

[81]  B. Galef The Biology of Traditions: “Traditional” foraging behaviors of brown and black rats ( Rattus norvegicus and Rattus rattus ) , 2003 .

[82]  L. Giraldeau,et al.  Social influences on foraging in vertebrates: causal mechanisms and adaptive functions , 2001, Animal Behaviour.

[83]  Kevin N Laland,et al.  The animal cultures debate. , 2006, Trends in ecology & evolution.

[84]  N. Davies,et al.  Social Transmission of a Host Defense Against Cuckoo Parasitism , 2009, Science.

[85]  Luke Rendell,et al.  Nine-spined sticklebacks deploy a hill-climbing social learning strategy , 2009 .

[86]  Kevin N. Laland,et al.  Social learning of foraging sites and escape routes in wild Trinidadian guppies , 2003, Animal Behaviour.

[87]  A. S. Griffin,et al.  Social learning about predators: a review and prospectus , 2004, Learning & behavior.

[88]  N. Davies,et al.  Learning fine-tunes a specific response of nestlings to the parental alarm calls of their own species , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[89]  Frank C Keil,et al.  The scope and limits of overimitation in the transmission of artefact culture , 2011, Philosophical Transactions of the Royal Society B: Biological Sciences.

[90]  K. Laland,et al.  From fish to fashion: experimental and theoretical insights into the evolution of culture , 2011, Philosophical Transactions of the Royal Society B: Biological Sciences.