Cultural Evolution: The Second Inheritance
Keywords:
Social learning, Cultural transmission, Animal culture, Cultural evolution, Non-genetic inheritanceAbstract
Abstract
Social learning allows individuals to acquire information from others, facilitating the spread of behaviors that can form stable traditions and animal cultures. This review examines the mechanisms and evolutionary consequences of cultural transmission in non-human animals, focusing primarily on primates, cetaceans, and birds. We analyze evidence across diverse biological contexts, including foraging strategies in orcas, migratory routes in cranes and whales, and vocal learning in songbirds and parrots. These examples demonstrate that behaviors previously attributed solely to instinct are often shaped by social inheritance. Furthermore, we explore how cultural evolution interacts with genetic evolution. Case studies, such as genomic adaptations in distinct orca ecotypes and accelerated speciation rates in vocal-learning bird lineages, suggest that culture can act as a selective pressure driving morphological and genetic divergence. We conclude that cultural transmission constitutes a secondary inheritance system complementary to genetics. Recognizing this dual inheritance model is essential for a comprehensive understanding of animal behavior, adaptation, and speciation.
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References
Allen, J., Weinrich, M., Hoppitt, W., Rendell, L. (2013). Network-based diffusion analysis reveals cultural transmission of lobtail feeding in humpback whales. Science, 340 (6131), 485–488. https://doi.org/10.1126/science.1231976
Aplin, L. (2016). Understanding the multiple factors governing social learning and the diffusion of innovations. Current Opinion in Behavioral Sciences, 12, 59–65. https://doi.org/10.1016/J.COBEHA.2016.09.003
Aplin, LM., Farine, DR., Morand-Ferron, J., Cockburn, A., Thornton, A., Sheldon, BC. (2014). Experimentally induced innovations lead to persistent culture via conformity in wild birds. Nature, 518, 538. https://doi.org/10.1038/nature13998
Baker, CS., Palumbi, SR., Lambertsen, RH., Weinrich, MT., Calambokidis, J., O’Brien, SJ. (1990). Influence of seasonal migration on geographic distribution of mitochondrial DNA haplotypes in humpback whales. Nature, 344 (6263), 238–240. https://doi.org/10.1038/344238a0
Balsby, TJS., Adams, DM. (2011). Vocal similarity and familiarity determine response to potential flock mates in orange-fronted conures (Psittacidae). Animal Behaviour, 81(5), 983–991. https://doi.org/10.1016/J.ANBEHAV.2011.01.034
Beans, C. (2017). Can animal culture drive evolution? Proceedings of the National Academy of Sciences, 114 (30), 7734–7737. https://doi.org/10.1073/pnas.1709475114
Beecher, MD., Brenowitz, EA. (2005). Functional aspects of song learning in songbirds. Trends in Ecology & Evolution, 20 (3), 143–149. https://doi.org/10.1016/J.TREE.2005.01.004
Berg, KS., Delgado, S., Okawa, R., Beissinger, SR., Bradbury, JW. (2011). Contact calls are used for individual mate recognition in free-ranging green-rumped parrotlets,Forpus passerinus. Animal Behaviour, 81 (1), 241–248. https://doi.org/10.1016/J.ANBEHAV.2010.10.012
Biro, D., Inoue-Nakamura, N., Tonooka, R., Yamakoshi, G., Sousa, C., Matsuzawa, T. (2003). Cultural innovation and transmission of tool use in wild chimpanzees: Evidence from field experiments. Animal Cognition, 6(4), 213–223. https://doi.org/10.1007/s10071-003-0183-x
Boyd, R., Richerson, PJ. (1985). Culture and the evolutionary process. University of Chicago Press.
Caldwell, MC., Caldwell, DK. (1965). Individualized whistle contours in bottle-nosed dolphins (Tursiops truncatus). Nature, 207(4995), 434–435. https://doi.org/10.1038/207434a0
Colbeck, GJ., Duchesne, P., Postma, LD., Lesage, V., Hammill, MO., Turgeon, J. (2013). Groups of related belugas (Delphinapterus leucas) travel together during their seasonal migrations in and around Hudson Bay. Proceedings of the Royal Society B: Biological Sciences, 280 (1752), 20122552. https://doi.org/10.1098/rspb.2012.2552
Curio, E., Ernst, U., Vieth, W. (1978). Cultural transmission of enemy recognition: One function of mobbing. Science, 202 (4370), 899–901. https://doi.org/10.1126/science.202.4370.899
Dukas, R. (2013). Effects of learning on evolution: Robustness, innovation and speciation. Animal Behaviour, 85 (5), 1023–1030. https://doi.org/10.1016/J.ANBEHAV.2012.12.030
Farabaugh, SM., Linzenbold, A., Dooling, RJ. (1994). Vocal plasticity in budgerigars (Melopsittacus undulatus): Evidence for social factors in the learning of contact calls. Journal of Comparative Psychology, 108 (1), 81–92.
Foote, AD., Vijay, N., Ávila-Arcos, MC., Baird, RW., Durban, JW., Fumagalli, M., Gibbs, RA., Hanson, MB., Korneliussen, TS., Martin, MD., Robertson, KM., Sousa, VC., Vieira, FG., Vinar, T., Wade, P., Worley, KC., Excoffier, L., Morin, PA., Gilbert, MTP., Wolf, JBW. (2016). Genome-culture coevolution promotes rapid divergence of killer whale ecotypes. Nature Communications, 7, 11693. https://doi.org/10.1038/ncomms11693
Futuyma, DJ. (2013). Evolution (3rd ed.). Sinauer Associates Inc. Galef, BG., Whiten, A. (2017). The comparative psychology of social learning, in: J. Call, GM. Burghardt, IM. Pepperberg, CT. Snowdon, T. Zentall (Eds.), A handbook of comparative psychology: Perception, learning, and cognition (pp. 411–439). American Psychological Association. https://doi.org/10.1037/0000012-019
Garland, EC., Goldizen, AW., Rekdahl, ML., Constantine, R., Garrigue, C., Hauser, ND., Poole, MM., Robbins, J., Noad, MJ. (2011). Dynamic horizontal cultural transmission of humpback whale song at the ocean basin scale. Current Biology, 21 (8), 687–691. https://doi.org/10.1016/J.CUB.2011.03.019
Haslam, M., Hernandez-Aguilar, A., Ling, V., Carvalho, S., de la Torre, I., DeStefano, A., Du, A., Hardy, B., Harris, J., Marchant, L., Matsuzawa, T., McGrew, W., Mercader, J., Mora, R., Petraglia, M., Roche, H., Visalberghi, E., Warren, R. (2009). Primate archaeology. Nature, 460 (7253), 339–344. https://doi.org/10.1038/nature08188
Heyes, CM. (2012). What’s social about social learning? Journal of Comparative Psychology, 126 (2), 193–202. https://doi.org/10.1037/a0025180
Heyes, CM. (1994). Social learning in animals: Categories and mechanisms. Biological Reviews of the Cambridge Philosophical Society, 69 (2), 207–231.
Heyes, CM., Galef Jr, BG. (1996). Social learning in animals: The roots of culture. Academic Press.
Itan, Y., Powell, A., Beaumont, MA., Burger, J., Thomas, MG. (2009). The origins of lactase persistence in Europe. PLoS Computational Biology, 5 (8), e1000491. https://doi.org/10.1371/journal.pcbi.1000491
Janik, VM., Slater, PJB. (1998). Context-specific use suggests that bottlenose dolphin signature whistles are cohesion calls. Animal Behaviour, 56 (4), 829–838. https://doi.org/10.1006/ANBE.1998.0881
Kawai, M. (1965). Newly-acquired pre-cultural behavior of the natural troop of Japanese monkeys on Koshima Islet. Primates, 6 (1), 1–30.
King, SL., Janik, VM. (2013). Bottlenose dolphins can use learned vocal labels to address each other. Proceedings of the National Academy of Sciences, 110(32), 13216–13221. https://doi.org/10.1073/pnas.1304459110
Laland, KN., Hoppitt, W. (2003). Do animals have culture? Evolutionary Anthropology: Issues, News, and Reviews, 12 (3), 150–159. https://doi.org/10.1002/evan.10111
Lishman, WA., Teets, T., Duff, JW., Sladen, WJL., Shire, GG., Goolsby, KM., Bezner, KWA., and Urbanek. RP. (1997) A reintroduction technique for migratory birds: leading Canada geese and isolation-reared sandhill cranes with ultralight aircraft, en: Urbanek RP, Stahlecker DW, eds. (1997). Proceedings of the Seventh North American Crane Workshop, 1996 Jan 10-13, Biloxi, Mississippi. Grand Island, NE: North American Crane Working Group. pp. 96-104.
Luncz, LV., Boesch, C. (2014). Tradition over trend: Neighboring chimpanzee communities maintain differences in cultural behavior despite frequent immigration of adult females. American Journal of Primatology, 76 (7), 649–657. https://doi.org/10.1002/ajp.22259
Mason, NA., Burns, KJ., Tobias, JA., Claramunt, S., Seddon, N., Derryberry, EP. (2017). Song evolution, speciation, and vocal learning in passerine birds. Evolution, 71 (3), 786–796. https://doi.org/10.1111/evo.13159
McGrew, WC., Tutin, CEG. (1978). Evidence for a social custom in wild chimpanzees? Man, 13 (2), 234–251.
Mercader, J., Barton, H., Gillespie, J., Harris, J., Kuhn, S., Tyler, R., Boesch, C. (2007). 4,300-year-old chimpanzee sites and the origins of percussive stone technology. Proceedings of the National Academy of Sciences, 104(9), 3043–3048. https://doi.org/10.1073/pnas.0607909104
Mesoudi, A. (2015). Cultural evolution: A review of theory, findings and controversies. Evolutionary Biology, 43(4), 481–497. https://doi.org/10.1007/s11692-015-9320-0
Mesoudi, A., Whiten, A., Laland, KN. (2006). Towards a unified science of cultural evolution. The Behavioral and Brain Sciences, 29 (4), 329–383. https://doi.org/10.1017/S0140525X06009083
Mueller, T., O’Hara, RB., Converse, SJ., Urbanek, RP., Fagan, WF. (2013). Social learning of migratory performance. Science, 341(6149), 999–1002. https://doi.org/10.1126/science.1237139
Mundinger, PC. (1980). Animal cultures and a general theory of cultural evolution. Ethology and Sociobiology,1 (3), 183–223 https://doi.org/10.1016/0162-3095(80)90008-4
Norton-Griffiths, M. (1967). Some ecological aspects of the feeding behaviour of the oystercatcher Haematopus ostralegus on the edible mussel Mytilus edulis. Ibis, 109(3), 412–424. https://doi.org/10.1111/j.1474-919X.1967.tb04014.x
Nottebohm, F. (1972). The origins of vocal learning. The American Naturalist, 106 (947), 116–140.
Palacín, C., Alonso, JC., Alonso, JA., Magaña, M., Martín, CA. (2011). Cultural transmission and flexibility of partial migration patterns in a long-lived bird, the great bustard Otis tarda. Journal of Avian Biology, 42(4), 301–308. https://doi.org/10.1111/j.1600-048X.2011.05395.x
Pipek, P., Petrusková, T., Petrusek, A., Diblíková, L., Eaton, MA., Pyšek, P. (2016). Dialects of an invasive songbird are preserved in its invaded but not native source range. Ecography, 41(2), 245–254. https://doi.org/10.1111/ecog.02779
Podos, J., Warren, PS. (2007). The evolution of geographic variation in birdsong. Advances in the Study of Behavior, 37, 403–458. https://doi.org/10.1016/S0065-3454(07)37009-5
Rendell, L., Whitehead, H. (2001). Culture in whales and dolphins. Behavioral and Brain Sciences, 24, 309–382.
Riesch, R., Barrett-Lennard, L. G., Ellis, G. M., Ford, J. K. B., Deecke, V. B. (2012). Cultural traditions and the evolution of reproductive isolation: Ecological speciation in killer whales? Biological Journal of the Linnean Society, 106 (1), 1–17. https://doi.org/10.1111/j.1095-8312.2012.01872.x
Robbins, MM., Ando, C., Fawcett, KA., Grueter, CC., Hedwig, D., Iwata, Y., Lodwick, JL., Masi, S., Salmi, R., Stoinski, TS., Todd, A., Vercellio, V., Yamagiwa, J. (2016). Behavioral variation in gorillas: Evidence of potential cultural traits. PLOS ONE, 11(9), e0160483. https://doi.org/10.1371/journal.pone.0160483
Scarl, J. C., Bradbury, J. W. (2009). Rapid vocal convergence in an Australian cockatoo, the galah Eolophus roseicapillus. Animal Behaviour, 77(5), 1019–1026. https://doi.org/10.1016/J.ANBEHAV.2008.11.024
Searcy, W. A., Andersson, M. (1986). Sexual selection and the evolution of song. Annual Review of Ecology and Systematics, 17 (1), 507–533. https://doi.org/10.1146/annurev.es.17.110186.002451
Sladen, WJL., Lishman, WA., Ellis, DH., Shire, GG., Rininger, DL. (2002). Teaching migration routes to Canada geese and Trumpeter swans using ultralight aircraft, 1990-2001. Proceedings of the North American Crane Workshop, 25.
Slagsvold, T., Wiebe, KL. (2011). Social learning in birds and its role in shaping a foraging niche. Philosophical Transactions of the Royal Society B: Biological Sciences, 366(1567), 969–977. https://doi.org/10.1098/rstb.2010.0343
Snell-Rood, EC. (2013). An overview of the evolutionary causes and consequences of behavioural plasticity. Animal Behaviour, 85 (5), 1004–1011. https://doi.org/10.1016/J.ANBEHAV.2012.12.031
Tyack, P. (1981). Interactions between singing Hawaiian humpback whales and conspecifics nearby. Behavioral Ecology and Sociobiology, 8 (2), 105–116. https://doi.org/10.1007/BF00300822
Valenzuela, LO., Sironi, M., Rowntree, VJ., Seger, J. (2009). Isotopic and genetic evidence for culturally inherited site fidelity to feeding grounds in southern right whales (Eubalaena australis). Molecular Ecology, 18(5), 782–791. https://doi.org/10.1111/j.1365-294X.2008.04069.x
van Schaik, CP., Ancrenaz, M., Borgen, G., Galdikas, B., Knott, CD., Singleton, I., Suzuki, A., Utami, SS., Merrill, M. (2003). Orangutan cultures and the evolution of material culture. Science, 299 (5603), 102–105. https://doi.org/10.1126/science.1078004
White, D. J. (2004). Influences of social learning on mate-choice decisions. Learning and Behavior, 32 (1), 105–113.
White, L. A. (1959). The concept of culture. American Anthropologist, 61 (2), 227–251.
Whitehead, H. (2007). Learning, climate and the evolution of cultural capacity. Journal of Theoretical Biology, 245 (2), 341–350. https://doi.org/10.1016/J.JTBI.2006.10.001
Whitehead, H. (2010). Conserving and managing animals that learn socially and share cultures. Learning Behavior, 38 (3), 329–336. https://doi.org/10.3758/LB.38.3.329
Whitehead, H., Richerson, P. J. (2009). The evolution of conformist social learning can cause population collapse in realistically variable environments. Evolution and Human Behavior, 30(4), 261–273. https://doi.org/10.1016/J.EVOLHUMBEHAV.2009.02.003
Whiten, A. (2005). The second inheritance system of chimpanzees and humans. Nature, 437(7055), 52–55. https://doi.org/10.1038/nature04023
Whiten, A. (2011). The scope of culture in chimpanzees, humans and ancestral apes. Philosophical Transactions of the Royal Society B: Biological Sciences, 366(1567), 997–1007. https://doi.org/10.1098/rstb.2010.0334
Whiten, A. (2017a). A second inheritance system: The extension of biology through culture. Interface Focus, 7 (5), 20160142. https://doi.org/10.1098/rsfs.2016.0142
Whiten, A. (2017b). Culture extends the scope of evolutionary biology in the great apes. Proceedings of the National Academy of Sciences, 114(30), 7790–7797. https://doi.org/10.1073/pnas.1620733114
Whiten, A. (2019). Cultural evolution in animals. Annual Review of Ecology, Evolution, and Systematics, 50, 1–22. https://doi.org/10.1146/annurev-ecolsys-110218-025040
Whiten, A., Goodall, J., McGrew, WC., Nishida, T., Reynolds, V., Sugiyama, Y., Tutin, C. EG., Wrangham, RW., Boesch, C. (1999). Cultures in chimpanzees. Nature, 399 (6737), 682–685. https://doi.org/10.1038/21415
Woodgate, JL., Mariette, MM., Bennett, ATD., Griffith, SC., Buchanan, K. L. (2012). Male song structure predicts reproductive success in a wild zebra finch population. Animal Behaviour, 83 (3), 773–781. https://doi.org/10.1016/J.ANBEHAV.2011.12.027
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