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The cognitive challenges of cooperation in human and nonhuman animals

Nature Reviews Psychology volume 2, pages 523–536 (2023)Cite this article

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A Publisher Correction to this article was published on 01 August 2023

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Abstract

Cooperation is widespread in nature, occurring in every taxa on Earth. Nevertheless, the contexts in which cooperation occurs — and the forms it takes — vary widely. In this Review, we outline how cooperation can evolve in nature and the cognition needed to support cooperation in different scenarios. We argue that the cognitively simplest forms of cooperation are those where an organism does not need to recognize interaction partners individually and that do not depend upon individuals keeping track of their partners’ actions and making contingent return investments. These simpler cooperative interactions occur most frequently among kin and among interdependent interaction partners and are relatively common in non-human animals. Conversely, cooperation involving individual recognition of interaction partners and where benefits depend upon contingent responses levy greater cognitive demands and occur in non-human animals only in limited contexts.

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Fig. 1: Pathways by which investments might yield benefits to an individual and their partner(s).
Fig. 2: Cooperative interactions categorized by how cognitive challenges are solved.

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References

  1. Bshary, R. & Bergmüller, R. Distinguishing four fundamental approaches to the evolution of helping. J. Evol. Biol. 21, 405–420 (2008).

    Article  PubMed  Google Scholar 

  2. West, S. A. & Gardner, A. Adaptation and inclusive fitness. Curr. Biol. 23, R577–R584 (2013).

    Article  PubMed  Google Scholar 

  3. Hamilton, W. The genetical evolution of social behaviour. I. J. Theor. Biol. 7, 1–16 (1964).

    Article  PubMed  Google Scholar 

  4. Hamilton, W. The genetical evolution of social behaviour. II. J. Theor. Biol. 7, 17–52 (1964).

    Article  PubMed  Google Scholar 

  5. Kay, T., Lehmann, L. & Keller, L. Kin selection and altruism. Curr. Biol. 29, R438–R442 (2019).

    Article  PubMed  Google Scholar 

  6. Bourke Andrew, F. G. Hamilton’s rule and the causes of social evolution. Phil. Trans. R. Soc. B 369, 20130362 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  7. Trivers, R. L. The evolution of reciprocal altruism. Q. Rev. Biol. 46, 35–57 (1971).

    Article  Google Scholar 

  8. Raihani, N. J. & Bshary, R. Resolving the iterated prisoner’s dilemma: theory and reality. J. Evol. Biol. 24, 1628–1639 (2011).

    Article  PubMed  Google Scholar 

  9. Taborsky, M., Frommen, J. G. & Riehl, C. Correlated pay-offs are key to cooperation. Phil. Trans. R. Soc. B 371, 20150084 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  10. Krams, I., Krama, T., Igaune, K. & Mänd, R. Experimental evidence of reciprocal altruism in the pied flycatcher. Behav. Ecol. Sociobiol. 62, 599–605 (2008).

    Article  Google Scholar 

  11. Roberts, G. et al. The benefits of being seen to help others: indirect reciprocity and reputation-based partner choice. Phil. Trans. R. Soc. B 376, 20200290 (2021).

    Article  PubMed  PubMed Central  Google Scholar 

  12. Kandori, M. Social norms and community enforcement. Rev. Econ. Stud. 59, 63–80 (1992).

    Article  Google Scholar 

  13. Manrique, H. M. et al. The psychological foundations of reputation-based cooperation. Phil. Trans. R. Soc. B 376, 20200287 (2021).

    Article  PubMed  PubMed Central  Google Scholar 

  14. Clutton-Brock, T. H. & Parker, G. A. Punishment in animal societies. Nature 373, 209–216 (1995).

    Article  PubMed  Google Scholar 

  15. Raihani, N. J., Thornton, A. & Bshary, R. Punishment and cooperation in nature. Trends Ecol. Evol. 27, 288–295 (2012).

    Article  PubMed  Google Scholar 

  16. Raihani, N. J. & Bshary, R. Punishment: one tool, many uses. Evol. Hum. Sci. 1, E12 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  17. Raihani, N. J. & Bshary, R. The reputation of punishers. Trends Ecol. Evol. 30, 98–103 (2015).

    Article  PubMed  Google Scholar 

  18. Bshary, R. & Grutter, A. S. Asymmetric cheating opportunities and partner control in a cleaner fish mutualism. Anim. Behav. 63, 547–555 (2002).

    Article  Google Scholar 

  19. Arseneau-Robar, T. J. M. et al. Female monkeys use both the carrot and the stick to promote male participation in intergroup fights. Proc. R. Soc. B 283, 20161817 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  20. Connor, R. C. Pseudo-reciprocity: investing in mutualism. Anim. Behav. 34, 1562–1566 (1986).

    Article  Google Scholar 

  21. Leimar, O. & Connor, R. By-product benefits, reciprocity, and pseudoreciprocity in mutualism. In Genetic And Cultural Evolution Of Cooperation (MIT Press, 2003).

  22. Nobre, T., Rouland-Lefèvre, C. & Aanen, D. K. Comparative biology of fungus cultivation in termites and ants. In Biology Of Termites: A Modern Synthesis (eds Bignell, D. E., Roisin, Y. & Lo, N.) 193–210 (Springer, 2011).

  23. Darden, S. K., James, R., Cave, J. M., Brask, J. B. & Croft, D. P. Trinidadian guppies use a social heuristic that can support cooperation among non-kin. Proc. R. Soc. B 287, 20200487 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  24. Wong, M. Y. L., Buston, P. M., Munday, P. L. & Jones, G. P. The threat of punishment enforces peaceful cooperation and stabilizes queues in a coral-reef fish. Proc. R. Soc. B 274, 1093–1099 (2007).

    Article  PubMed  PubMed Central  Google Scholar 

  25. Roberts, G. Cooperation through interdependence. Anim. Behav. 70, 901–908 (2005).

    Article  Google Scholar 

  26. Aktipis, A. et al. Understanding cooperation through fitness interdependence. Nat. Hum. Behav. 2, 429–431 (2018).

    Article  PubMed  Google Scholar 

  27. Bshary, R., Zuberbühler, K. & van Schaik, C. P. Why mutual helping in most natural systems is neither conflict-free nor based on maximal conflict. Phil. Trans. R. Soc. B 371, 20150091 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  28. Barclay, P. Reciprocity creates a stake in one’s partner, or why you should cooperate even when anonymous. Proc. R. Soc. B 287, 20200819 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  29. Raihani, N. The Social Instinct: How Cooperation Shaped The World (Random House, 2021).

  30. Kramer, K. L. & Russell, A. F. Kin-selected cooperation without lifetime monogamy: human insights and animal implications. Trends Ecol. Evol. 29, 600–606 (2014).

    Article  PubMed  Google Scholar 

  31. Jaeggi, A. V. & Gurven, M. Reciprocity explains food sharing in humans and other primates independent of kin selection and tolerated scrounging: a phylogenetic meta-analysis. Proc. R. Soc. B 280, 20131615 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  32. Milinski, M., Semmann, D. & Krambeck, H. Donors to charity gain in both indirect reciprocity and political reputation. Proc. R. Soc. Lond. B 269, 881 (2002).

    Article  Google Scholar 

  33. Sommerfeld, R. D., Krambeck, H.-J., Semmann, D. & Milinski, M. Gossip as an alternative for direct observation in games of indirect reciprocity. Proc. Natl Acad. Sci. USA 104, 17435–17440 (2007).

    Article  PubMed  PubMed Central  Google Scholar 

  34. Shogren, E. H. & Boyle, W. A. Spread the word: male manakins advertise the presence of display sites with neighbouring competitors. Anim. Behav. 177, 147–158 (2021).

    Article  Google Scholar 

  35. Graw, B. & Manser, M. B. The function of mobbing in cooperative meerkats. Anim. Behav. 74, 507–517 (2007).

    Article  Google Scholar 

  36. Bennett, N. C. & Faulkes, C. G. African Mole-Rats: Ecology And Eusociality (Cambridge Univ. Press, 2000).

  37. Stacey, P. B. & Koenig, W. D. Cooperative breeding in the acorn woodpecker. Sci. Am. 251, 114–121 (1984).

    Article  Google Scholar 

  38. Vail, A. L., Manica, A. & Bshary, R. Referential gestures in fish collaborative hunting. Nat. Commun. 4, 1765 (2013).

    Article  PubMed  Google Scholar 

  39. Bell, M. B. V. Cooperative begging in banded mongoose pups. Curr. Biol. 17, 717–721 (2007).

    Article  PubMed  Google Scholar 

  40. Brown, J. L. Cooperation—a biologist’s dilemma. In Advances In The Study Behavior Vol. 13 (eds Rosenblatt, J. S., Hinde, R. A., Beer, C. & Busnel, M.-C.) 1–37 (Academic Press, 1983).

  41. Bshary, A. & Bshary, R. Self-serving punishment of a common enemy creates a public good in reef fishes. Curr. Biol. 20, 2032–2035 (2010).

    Article  PubMed  Google Scholar 

  42. Koenig, W. D., Walters, E. L. & Barve, S. Does helping-at-the-nest help? The case of the acorn woodpecker. Front. Ecol. Evol. 7, 272 (2019).

    Article  Google Scholar 

  43. Kokko, H., Johnstone, R. A. & Clutton-Brock, T. H. The evolution of cooperative breeding through group augmentation. Proc. R. Soc. Lond. B 268, 187–196 (2001).

    Article  Google Scholar 

  44. Gilby, I. C. et al. ‘Impact hunters’ catalyse cooperative hunting in two wild chimpanzee communities. Phil. Trans. R. Soc. B 370, 20150005 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  45. Gilby, I. C., Eberly, L. E. & Wrangham, R. W. Economic profitability of social predation among wild chimpanzees: individual variation promotes cooperation. Anim. Behav. 75, 351–360 (2008).

    Article  Google Scholar 

  46. Watts, D. P. & Mitani, J. C. Hunting behavior of chimpanzees at Ngogo, Kibale National Park, Uganda. Int. J. Primatol. https://doi.org/10.1023/A:1013270606320 (2002).

    Article  Google Scholar 

  47. Duguid, S. & Melis, A. P. How animals collaborate: underlying proximate mechanisms. WIREs Cogn. Sci. 11, e1529 (2020).

    Article  Google Scholar 

  48. Burton-Chellew, M. N., May, R. M. & West, S. A. Combined inequality in wealth and risk leads to disaster in the climate change game. Clim. Change 120, 815–830 (2013).

    Article  Google Scholar 

  49. Hauser, O. P., Rand, D. G., Peysakhovich, A. & Nowak, M. A. Cooperating with the future. Nature 511, 220–223 (2014).

    Article  PubMed  Google Scholar 

  50. Vasconcelos, V. V., Santos, F. C., Pacheco, J. M. & Levin, S. A. Climate policies under wealth inequality. Proc. Natl Acad. Sci. USA 111, 2212–2216 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  51. Gatiso, T. T., Vollan, B. & Nuppenau, E.-A. Resource scarcity and democratic elections in commons dilemmas: an experiment on forest use in Ethiopia. Ecol. Econ. 114, 199–207 (2015).

    Article  Google Scholar 

  52. Gatiso, T. T. & Vollan, B. Democracy and cooperation in commons management: experimental evidence of representative and direct democracy from community forests in Ethiopia. Environ. Dev. Econ. 22, 110–132 (2017).

    Article  Google Scholar 

  53. Kosfeld, M. & Rustagi, D. Leader punishment and cooperation in groups: experimental field evidence from commons management in Ethiopia. Am. Econ. Rev. 105, 747–783 (2015).

    Article  Google Scholar 

  54. Rustagi, D., Engel, S. & Kosfeld, M. Conditional cooperation and costly monitoring explain success in forest commons management. Science 330, 961–965 (2010).

    Article  PubMed  Google Scholar 

  55. Yoeli, E., Hoffman, M., Rand, D. G. & Nowak, M. A. Powering up with indirect reciprocity in a large-scale field experiment. Proc. Natl Acad. Sci. USA 110, 10424–10429 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  56. Andreoni, J. & Petrie, R. Public goods experiments without confidentiality: a glimpse into fund-raising. J. Public Econ. 88, 1605–1623 (2004).

    Article  Google Scholar 

  57. Mateo, J. M. Recognition systems and biological organization: the perception component of social recognition. Ann. Zool. Fenn. 41, 729–745 (2004).

    Google Scholar 

  58. Leedale, A. E., Li, J. & Hatchwell, B. J. Kith or kin? Familiarity as a cue to kinship in social birds. Front. Ecol. Evol. 8, 00077 (2020).

    Article  Google Scholar 

  59. Duncan, C., Gaynor, D., Clutton-Brock, T. & Dyble, M. The evolution of indiscriminate altruism in a cooperatively breeding mammal. Am. Nat. 193, 841–851 (2019).

    Article  PubMed  Google Scholar 

  60. Frank, E. T., Wehrhahn, M. & Linsenmair, K. E. Wound treatment and selective help in a termite-hunting ant. Proc. R. Soc. B 285, 20172457 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  61. Miler, K. Moribund ants do not call for help. PLoS ONE 11, e0151925 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  62. Roche, D. G., Jornod, M., Douet, V., Grutter, A. S. & Bshary, R. Client fish traits underlying variation in service quality in a marine cleaning mutualism. Anim. Behav. 175, 137–151 (2021).

    Article  Google Scholar 

  63. Fischer, E. A. The relationship between mating system and simultaneous hermaphroditism in the coral reef fish, Hypoplectrus nigricans (Serranidae). Anim. Behav. 28, 620–633 (1980).

    Article  Google Scholar 

  64. Aktipis, C. A. Know when to walk away: contingent movement and the evolution of cooperation. J. Theor. Biol. 231, 249–260 (2004).

    Article  PubMed  Google Scholar 

  65. Melis, A. P., Hare, B. & Tomasello, M. Chimpanzees recruit the best collaborators. Science 311, 1297 (2006).

    Article  PubMed  Google Scholar 

  66. Bshary, R., Hohner, A., Ait-el-Djoudi, K. & Fricke, H. Interspecific communicative and coordinated hunting between groupers and giant moray eels in the Red Sea. PLoS Biol. 4, e431 (2006).

    Article  PubMed  PubMed Central  Google Scholar 

  67. Vail, A. L., Manica, A. & Bshary, R. Fish choose appropriately when and with whom to collaborate. Curr. Biol. 24, R791–R793 (2014).

    Article  PubMed  Google Scholar 

  68. Gilby, I. C. & Machanda, Z. P. Advanced cognition in wild chimpanzees: lessons from observational studies. Curr. Opin. Behav. Sci. 46, 101183 (2022).

    Article  Google Scholar 

  69. Johnsson, J. I. & Åkerman, A. Watch and learn: preview of the fighting ability of opponents alters contest behaviour in rainbow trout. Anim. Behav. 56, 771–776 (1998).

    Article  PubMed  Google Scholar 

  70. Paz-y-Miño C, G., Bond, A. B., Kamil, A. C. & Balda, R. P. Pinyon jays use transitive inference to predict social dominance. Nature 430, 778–781 (2004).

    Article  PubMed  Google Scholar 

  71. Abdai, J. & Miklósi, Á. The origin of social evaluation, social eavesdropping, reputation formation, image scoring or what you will. Front. Psychol. 7, 1772 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  72. Bshary, R. & Grutter, A. S. Image scoring and cooperation in a cleaner fish mutualism. Nature 441, 975–978 (2006).

    Article  PubMed  Google Scholar 

  73. Chijiiwa, H., Kuroshima, H., Hori, Y., Anderson, J. R. & Fujita, K. Dogs avoid people who behave negatively to their owner: third-party affective evaluation. Anim. Behav. 106, 123–127 (2015).

    Article  Google Scholar 

  74. Russell, Y. I., Call, J. & Dunbar, R. I. M. Image scoring in great apes. Behav. Process. 78, 108–111 (2008).

    Article  Google Scholar 

  75. Subiaul, F., Vonk, J., Okamoto-Barth, S. & Barth, J. Do chimpanzees learn reputation by observation? Evidence from direct and indirect experience with generous and selfish strangers. Anim. Cogn. 11, 611–623 (2008).

    Article  PubMed  Google Scholar 

  76. Herrmann, E., Keupp, S., Hare, B., Vaish, A. & Tomasello, M. Direct and indirect reputation formation in nonhuman great apes (Pan paniscus, Pan troglodytes, Gorilla gorilla, Pongo pygmaeus) and human children (Homo sapiens). J. Comp. Psychol. 127, 63–75 (2013).

    Article  PubMed  Google Scholar 

  77. Anderson, J. R., Kuroshima, H., Takimoto, A. & Fujita, K. Third-party social evaluation of humans by monkeys. Nat. Commun. 4, 1561 (2013).

    Article  PubMed  Google Scholar 

  78. Kawai, N., Yasue, M., Banno, T. & Ichinohe, N. Marmoset monkeys evaluate third-party reciprocity. Biol. Lett. 10, 20140058 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  79. Krupenye, C. & Hare, B. Bonobos prefer individuals that hinder others over those that help. Curr. Biol. 28, 280–286.e5 (2018).

    Article  PubMed  Google Scholar 

  80. Kundey, S. M. A. et al. Reputation-like inference in domestic dogs (Canis familiaris). Anim. Cogn. 14, 291–302 (2011).

    Article  PubMed  Google Scholar 

  81. Marshall-Pescini, S., Passalacqua, C., Ferrario, A., Valsecchi, P. & Prato-Previde, E. Social eavesdropping in the domestic dog. Anim. Behav. 81, 1177–1183 (2011).

    Article  Google Scholar 

  82. Nitzschner, M., Kaminski, J., Melis, A. & Tomasello, M. Side matters: potential mechanisms underlying dogs’ performance in a social eavesdropping paradigm. Anim. Behav. 90, 263–271 (2014).

    Article  Google Scholar 

  83. Dahl, A., Schuck, R. K. & Campos, J. J. Do young toddlers act on their social preferences? Dev. Psychol. 49, 1964–1970 (2013).

    Article  PubMed  Google Scholar 

  84. Vaish, A., Carpenter, M. & Tomasello, M. Young children selectively avoid helping people with harmful intentions. Child Dev. 81, 1661–1669 (2010).

    Article  PubMed  Google Scholar 

  85. Hamlin, J. K. & Wynn, K. Young infants prefer prosocial to antisocial others. Cogn. Dev. 26, 30–39 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  86. Hamlin, J. K., Wynn, K. & Bloom, P. Social evaluation by preverbal infants. Nature 450, 557–559 (2007).

    Article  PubMed  Google Scholar 

  87. Margoni, F. & Surian, L. Infants’ evaluation of prosocial and antisocial agents: a meta-analysis. Dev. Psychol. 54, 1445–1455 (2018).

    Article  PubMed  Google Scholar 

  88. Nighbor, T., Kohn, C., Normand, M. & Schlinger, H. Stability of infants’ preference for prosocial others: implications for research based on single-choice paradigms. PLoS ONE 12, e0178818 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  89. Salvadori, E. et al. Probing the strength of infants’ preference for helpers over hinderers: two replication attempts of Hamlin and Wynn (2011). PLoS ONE 10, e0140570 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  90. Schlingloff, L., Csibra, G. & Tatone, D. Do 15-month-old infants prefer helpers? A replication of Hamlin et al. (2007). R. Soc. Open. Sci. 7, 191795 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  91. Johnstone, R. A. et al. Reciprocity and conditional cooperation between great tit parents. Behav. Ecol. 25, 216–222 (2014).

    Article  Google Scholar 

  92. Taborsky, M., Frommen, J. G. & Riehl, C. The evolution of cooperation based on direct fitness benefits. Phil. Trans. R. Soc. B 371, 20150472 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  93. Müller, J. J. A., Massen, J. J. M., Bugnyar, T. & Osvath, M. Ravens remember the nature of a single reciprocal interaction sequence over 2 days and even after a month. Anim. Behav. 128, 69–78 (2017).

    Article  Google Scholar 

  94. Fraser, O. N. & Bugnyar, T. Reciprocity of agonistic support in ravens. Anim. Behav. 83, 171–177 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  95. Schweinfurth, M. K. & Call, J. Revisiting the possibility of reciprocal help in non-human primates. Neurosci. Biobehav. Rev. 104, 73–86 (2019).

    Article  PubMed  Google Scholar 

  96. Schweinfurth, M. K. & Taborsky, M. Reciprocal trading of different commodities in Norway rats. Curr. Biol. 28, 594–599 (2018).

    Article  PubMed  Google Scholar 

  97. Kettler, N., Schweinfurth, M. K. & Taborsky, M. Rats show direct reciprocity when interacting with multiple partners. Sci. Rep. 11, 3228 (2021).

    Article  PubMed  PubMed Central  Google Scholar 

  98. Schweinfurth, M. K. et al. Do female Norway rats form social bonds? Behav. Ecol. Sociobiol. 71, 98 (2017).

    Article  Google Scholar 

  99. Schweinfurth, M. K. & Taborsky, M. Rats play tit-for-tat instead of integrating social experience over multiple interactions. Proc. R. Soc. B 287, 20192423 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  100. Lewis, A., Berntsen, D. & Call, J. Long-term memory of past events in great apes. Curr. Dir. Psychol. Sci. 28, 117–123 (2019).

    Article  Google Scholar 

  101. Martin-Ordas, G., Berntsen, D. & Call, J. Memory for distant past events in chimpanzees and orangutans. Curr. Biol. 23, 1438–1441 (2013).

    Article  PubMed  Google Scholar 

  102. Lewis, A., Bernsten, D. & Call, J. Remembering past exchanges: apes fail to use social cues. Anim. Behav. Cogn. https://doi.org/10.26451/abc.05.01.03.2018 (2018).

    Article  Google Scholar 

  103. Schwartz, B. L., Colon, M. R., Sanchez, I. C., Rodriguez, I. & Evans, S. Single-trial learning of ‘what’ and ‘who’ information in a gorilla (Gorilla gorilla gorilla): implications for episodic memory. Anim. Cogn. 5, 85–90 (2002).

    Article  PubMed  Google Scholar 

  104. Silk, J. B. Cooperation without counting: the puzzle of friendship. In Genetic And Cultural Evolution Of Cooperation (ed. Hammerstein, P.) 37–54 (MIT Press, 2003).

  105. Martin-Ordas, G., Haun, D., Colmenares, F. & Call, J. Keeping track of time: evidence for episodic-like memory in great apes. Anim. Cogn. 13, 331–340 (2010).

    Article  PubMed  Google Scholar 

  106. Carlson, N. V., Kelly, E. M. & Couzin, I. Individual vocal recognition across taxa: a review of the literature and a look into the future. Phil. Trans. R. Soc. B 375, 20190479 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  107. Parr, L. A. The evolution of face processing in primates. Phil. Trans. R. Soc. B 366, 1764–1777 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  108. Mendes, N. & Call, J. Chimpanzees form long-term memories for food locations after limited exposure. Am. J. Primatol. 76, 485–495 (2014).

    Article  PubMed  Google Scholar 

  109. Berghänel, A., Ostner, J., Schröder, U. & Schülke, O. Social bonds predict future cooperation in male Barbary macaques, Macaca sylvanus. Anim. Behav. 81, 1109–1116 (2011).

    Article  Google Scholar 

  110. Mitani, J. C. Male chimpanzees form enduring and equitable social bonds. Anim. Behav. 77, 633–640 (2009).

    Article  Google Scholar 

  111. Schino, G. & Aureli, F. Grooming reciprocation among female primates: a meta-analysis. Biol. Lett. 4, 9–11 (2008).

    Article  PubMed  Google Scholar 

  112. Brosnan, S. F. & de Waal, F. B. M. A proximate perspective on reciprocal altruism. Hum. Nat. 13, 129–152 (2002).

    Article  PubMed  Google Scholar 

  113. Schino, G. & Aureli, F. The relative roles of kinship and reciprocity in explaining primate altruism. Ecol. Lett. 13, 45–50 (2010).

    Article  PubMed  Google Scholar 

  114. Silk, J. B. The evolution of cooperation in primate groups. In Moral Sentiments And Material Interests: The Foundations Of Cooperation In Economic Life 43–73 (MIT Press, 2005).

  115. Jensen, K., Call, J. & Tomasello, M. Chimpanzees are vengeful but not spiteful. Proc. Natl Acad. Sci. USA 104, 13046–13050 (2007).

    Article  PubMed  PubMed Central  Google Scholar 

  116. Aureli, F., Cozzolino, R., Cordischi, C. & Scucchi, S. Kin-oriented redirection among Japanese macaques: an expression of a revenge system? Anim. Behav. 44, 283–291 (1992).

    Article  Google Scholar 

  117. Tiddi, B., di Sorrentino, E. P., Fischer, J. & Schino, G. Acquisition and functional consequences of social knowledge in macaques. R. Soc. Open Sci. 4, 160639 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  118. Bshary, R. & Schäffer, D. Choosy reef fish select cleaner fish that provide high-quality service. Anim. Behav. 63, 557–564 (2002).

    Article  Google Scholar 

  119. Raihani, N. J., Grutter, A. S. & Bshary, R. Punishers benefit from third-party punishment in fish. Science 327, 171–171 (2010).

    Article  PubMed  Google Scholar 

  120. Fehr, E. & Gächter, S. Altruistic punishment in humans. Nature 415, 137–140 (2002).

    Article  PubMed  Google Scholar 

  121. Fehr, E. & Fischbacher, U. Third-party punishment and social norms. Evol. Hum. Behav. 25, 63–87 (2004).

    Article  Google Scholar 

  122. Henrich, J. et al. Costly punishment across human societies. Science 312, 1767–1770 (2006).

    Article  PubMed  Google Scholar 

  123. Salali, G. D., Juda, M. & Henrich, J. Transmission and development of costly punishment in children. Evol. Hum. Behav. 36, 86–94 (2015).

    Article  Google Scholar 

  124. Kern, J. M. & Radford, A. N. Experimental evidence for delayed contingent cooperation among wild dwarf mongooses. Proc. Natl Acad. Sci. USA 115, 6255–6260 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  125. Hare, B., Melis, A. P., Woods, V., Hastings, S. & Wrangham, R. Tolerance allows bonobos to outperform chimpanzees on a cooperative task. Curr. Biol. 17, 619–623 (2007).

    Article  PubMed  Google Scholar 

  126. Tennie, C., Gilby, I. C. & Mundry, R. The meat-scrap hypothesis: small quantities of meat may promote cooperative hunting in wild chimpanzees (Pan troglodytes). Behav. Ecol. Sociobiol. 63, 421–431 (2009).

    Article  Google Scholar 

  127. Petit, O., Desportes, C. & Thierry, B. Differential probability of “coproduction” in two species of macaque (Macaca tonkeana, M. mulatta). Ethology 90, 107–120 (1992).

    Article  Google Scholar 

  128. Staes, N. et al. Drivers of dyadic cofeeding tolerance in Pan: a composite measure approach. Biology 11, 713 (2022).

    Article  PubMed  PubMed Central  Google Scholar 

  129. Wiltermuth, S. S. & Heath, C. Synchrony and cooperation. Psychol. Sci. 20, 1–5 (2009).

    Article  PubMed  Google Scholar 

  130. Wolf, W. & Tomasello, M. Visually attending to a video together facilitates great ape social closeness. Proc. R. Soc. B 286, 20190488 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  131. de Waal, F. B. M. & Berger, M. L. Payment for labour in monkeys. Nature 404, 563–563 (2000).

    Article  PubMed  Google Scholar 

  132. Boesch, C. & Boesch, H. Hunting behavior of wild chimpanzees in the Taï National Park. Am. J. Phys. Anthropol. 78, 547–573 (1989).

    Article  PubMed  Google Scholar 

  133. Boesch, C. Cooperative hunting in wild chimpanzees. Anim. Behav. 48, 653–667 (1994).

    Article  Google Scholar 

  134. Samuni, L., Preis, A., Deschner, T., Crockford, C. & Wittig, R. M. Reward of labor coordination and hunting success in wild chimpanzees. Commun. Biol. 1, 1–9 (2018).

    Article  Google Scholar 

  135. John, M., Duguid, S., Tomasello, M. & Melis, A. P. How chimpanzees (Pan troglodytes) share the spoils with collaborators and bystanders. PLoS ONE 14, e0222795 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  136. Melis, A. P., Schneider, A.-C. & Tomasello, M. Chimpanzees, Pan troglodytes, share food in the same way after collaborative and individual food acquisition. Anim. Behav. 82, 485–493 (2011).

    Article  Google Scholar 

  137. Gilby, I. C. Meat sharing among the Gombe chimpanzees: harassment and reciprocal exchange. Anim. Behav. 71, 953–963 (2006).

    Article  Google Scholar 

  138. Hamann, K., Bender, J. & Tomasello, M. Meritocratic sharing is based on collaboration in 3-year-olds. Dev. Psychol. 50, 121–128 (2014).

    Article  PubMed  Google Scholar 

  139. Melis, A. P., Altrichter, K. & Tomasello, M. Allocation of resources to collaborators and free-riders in 3-year-olds. J. Exp. Child. Psychol. 114, 364–370 (2013).

    Article  PubMed  Google Scholar 

  140. Ritov, O., Völter, C., Raihani, N. & Engelmann, J. Are nonhuman animals averse to inequity? A meta-analysis. Preprint at PsyArXiv https://doi.org/10.31234/osf.io/86vkf (2023).

  141. de Waal, F. B. M. Putting the altruism back into altruism: the evolution of empathy. Annu. Rev. Psychol. 59, 279–300 (2008).

    Article  PubMed  Google Scholar 

  142. Melis, A. P., Grocke, P., Kalbitz, J. & Tomasello, M. One for you, one for me: humans’ unique turn-taking skills. Psychol. Sci. 27, 987–996 (2016).

    Article  PubMed  Google Scholar 

  143. Warneken, F., Sebastián-Enesco, C., Benjamin, N. E. & Pieloch, K. A. Pay to play: children’s emerging ability to use acts of generosity for selfish ends. J. Exp. Child. Psychol. 188, 104675 (2019).

    Article  PubMed  Google Scholar 

  144. Sebastián-Enesco, C. & Warneken, F. The shadow of the future: 5-year-olds, but not 3-year-olds, adjust their sharing in anticipation of reciprocation. J. Exp. Child. Psychol. 129, 40–54 (2015).

    Article  PubMed  Google Scholar 

  145. Dunfield, K. A. & Kuhlmeier, V. A. Intention-mediated selective helping in infancy. Psychol. Sci. 21, 523–527 (2010).

    Article  PubMed  Google Scholar 

  146. Warneken, F. & Tomasello, M. The emergence of contingent reciprocity in young children. J. Exp. Child. Psychol. 116, 338–350 (2013).

    Article  PubMed  Google Scholar 

  147. Schino, G., Ferrario, V. & Addessi, E. Do capuchin monkeys engage in calculated reciprocity? Anim. Behav. 178, 141–148 (2021).

    Article  Google Scholar 

  148. Pinto, A., Oates, J., Grutter, A. S. & Bshary, R. Cleaner wrasses Labroides dimidiatus are more cooperative in the presence of an audience. Curr. Biol. 21, 1140–1144 (2011).

    Article  PubMed  Google Scholar 

  149. Grutter, A. S. Parasite removal rates by the cleaner wrasse Labroides dimidiatus. Mar. Ecol. Prog. Ser. 130, 61–70 (1996).

    Article  Google Scholar 

  150. Engelmann, J. M., Herrmann, E. & Tomasello, M. Five-year olds, but not chimpanzees, attempt to manage their reputations. PLoS ONE 7, e48433 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  151. Engelmann, J. M., Herrmann, E. & Tomasello, M. The effects of being watched on resource acquisition in chimpanzees and human children. Anim. Cogn. 19, 147–151 (2016).

    Article  PubMed  Google Scholar 

  152. Apicella, C. L. & Silk, J. B. The evolution of human cooperation. Curr. Biol. 29, R447–R450 (2019).

    Article  PubMed  Google Scholar 

  153. Melis, A. P. & Semmann, D. How is human cooperation different? Phil. Trans. R. Soc. B 365, 2663–2674 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  154. Hooper, P. L., Kaplan, H. S. & Jaeggi, A. V. Gains to cooperation drive the evolution of egalitarianism. Nat. Hum. Behav. 5, 847–856 (2021).

    Article  PubMed  Google Scholar 

  155. Tomasello, M., Melis, A. P., Tennie, C., Wyman, E. & Herrmann, E. Two key steps in the evolution of human cooperation: the interdependence hypothesis. Curr. Anthropol. 53, 673–692 (2012).

    Article  Google Scholar 

  156. Krupenye, C. & Call, J. Theory of mind in animals: current and future directions. WIREs Cogn. Sci. 10, e1503 (2019).

    Article  Google Scholar 

  157. Tomasello, M., Carpenter, M., Call, J., Behne, T. & Moll, H. Understanding and sharing intentions: the origins of cultural cognition. Behav. Brain Sci. 28, 675–691 (2005).

    Article  PubMed  Google Scholar 

  158. Hamann, K., Warneken, F., Greenberg, J. R. & Tomasello, M. Collaboration encourages equal sharing in children but not in chimpanzees. Nature 476, 328–331 (2011).

    Article  PubMed  Google Scholar 

  159. Dawes, C. T., Fowler, J. H., Johnson, T., McElreath, R. & Smirnov, O. Egalitarian motives in humans. Nature 446, 794–796 (2007).

    Article  PubMed  Google Scholar 

  160. Banerjee, R., Heyman, G. D. & Lee, K. The development of moral self-presentation. In The Oxford Handbook Of Moral Development (ed. Jensen, L. A.) 91–109 (Oxford Univ. Press, 2020).

  161. Blake, P. R., Rand, D. G., Tingley, D. & Warneken, F. The shadow of the future promotes cooperation in a repeated prisoner’s dilemma for children. Sci. Rep. 5, 14559 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  162. Engelmann, J. M. & Rapp, D. J. The influence of reputational concerns on children’s prosociality. Curr. Opin. Psychol. 20, 92–95 (2018).

    Article  PubMed  Google Scholar 

  163. McAuliffe, K., Blake, P. R., Steinbeis, N. & Warneken, F. The developmental foundations of human fairness. Nat. Hum. Behav. 1, 0042 (2017).

    Article  Google Scholar 

  164. Manrique, H. M. & Walker, M. J. Early Evolution Of Human Memory (Springer, 2017).

  165. Knofe, H., Engelmann, J., Tomasello, M. & Herrmann, E. Chimpanzees monopolize and children take turns in a limited resource problem. Sci. Rep. 9, 7597 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  166. Powers Simon, T., van Schaik Carel, P. & Lehmann, L. How institutions shaped the last major evolutionary transition to large-scale human societies. Phil. Trans. R. Soc. B 371, 20150098 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  167. Glowacki, L. & Lew-Levy, S. How small-scale societies achieve large-scale cooperation. Curr. Opin. Psychol. 44, 44–48 (2022).

    Article  PubMed  Google Scholar 

  168. Fehr, E. & Schurtenberger, I. Normative foundations of human cooperation. Nat. Hum. Behav. 2, 458–468 (2018).

    Article  PubMed  Google Scholar 

  169. House, B. R. et al. Social norms and cultural diversity in the development of third-party punishment. Proc. R. Soc. B 287, 20192794 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  170. Theriault, J. E., Young, L. & Barrett, L. F. The sense of should: a biologically-based framework for modeling social pressure. Phys. Life Rev. 36, 100–136 (2021).

    Article  PubMed  Google Scholar 

  171. Rakoczy, H., Warneken, F. & Tomasello, M. The sources of normativity: young children’s awareness of the normative structure of games. Dev. Psychol. 44, 875–881 (2008).

    Article  PubMed  Google Scholar 

  172. Andreoni, J. Impure altruism and donations to public goods: a theory of warm-glow giving. Econ. J. 100, 464–477 (1990).

    Article  Google Scholar 

  173. Harbaugh, W. T., Mayr, U. & Burghart, D. R. Neural responses to taxation and voluntary giving reveal motives for charitable donations. Science 316, 1622–1625 (2007).

    Article  PubMed  Google Scholar 

  174. Morris, A. & Cushman, F. A common framework for theories of norm compliance. Soc. Phil. Policy 35, 101–127 (2018).

    Article  Google Scholar 

  175. Barrett, L., Henzi, P. & Rendall, D. Social brains, simple minds: does social complexity really require cognitive complexity? Phil. Trans. R. Soc. B 362, 561–575 (2007).

    Article  PubMed  PubMed Central  Google Scholar 

  176. Raihani, N. J. Cognitive demands of sociality: from simple mechanisms to complex behaviour. J. Zool. 295, 1–3 (2015).

    Article  Google Scholar 

  177. Koenig, W. D. & Dickinson, J. L. Cooperative Breeding In Vertebrates (Cambridge Univ. Press, 2016).

  178. Wilson, E. O. Social insects. Science 172, 406–406 (1971).

    Article  PubMed  Google Scholar 

  179. Snowdon, C. T. Infant care in cooperatively breeding species. In Advances In The Study Of Behavior Vol. 25 (eds Rosenblatt, J. S. & Snowdon, C. T.) 643–689 (Academic Press, 1996).

  180. Kramer, K. L. Cooperative breeding and its significance to the demographic success of humans. Annu. Rev. Anthropol. 39, 417–436 (2010).

    Article  Google Scholar 

  181. Wiessner, P. Hunting, healing, and hxaro exchange: a long-term perspective on !Kung (Ju/’hoansi) large-game hunting. Evol. Hum. Behav. 23, 407–436 (2002).

    Article  Google Scholar 

  182. Fischer, E. A. Simultaneous hermaphroditism, tit-for-tat, and the evolutionary stability of social systems. Ethol. Sociobiol. 9, 119–136 (1988).

    Article  Google Scholar 

  183. Milinski, M., Pfluger, D., Külling, D. & Kettler, R. Do sticklebacks cooperate repeatedly in reciprocal pairs? Behav. Ecol. Sociobiol. 27, 17–21 (1990).

    Article  Google Scholar 

  184. Ringen, E. J., Duda, P. & Jaeggi, A. V. The evolution of daily food sharing: a Bayesian phylogenetic analysis. Evol. Hum. Behav. https://doi.org/10.1016/j.evolhumbehav.2019.04.003 (2019).

    Article  Google Scholar 

  185. Pedersen, E. J., Kurzban, R. & McCullough, M. E. Do humans really punish altruistically? A closer look. Proc. R. Soc. B 280, 20122723 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  186. Bailey, I., Myatt, J. P. & Wilson, A. M. Group hunting within the Carnivora: physiological, cognitive and environmental influences on strategy and cooperation. Behav. Ecol. Sociobiol. 67, 1–17 (2013).

    Article  Google Scholar 

  187. Wrangham, R. W. & Glowacki, L. Intergroup aggression in chimpanzees and war in nomadic hunter-gatherers. Hum. Nat. 23, 5–29 (2012).

    Article  PubMed  Google Scholar 

  188. Bradley, A., Lawrence, C. & Ferguson, E. Does observability affect prosociality? Proc. R. Soc. B 285, 20180116 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  189. Wu, J., Luan, S. & Raihani, N. Reward, punishment, and prosocial behavior: recent developments and implications. Curr. Opin. Psychol. 44, 117–123 (2022).

    Article  PubMed  Google Scholar 

  190. Diekmann, A. Volunteer’s dilemma. J. Confl. Resolut. 29, 605–610 (1985).

    Article  Google Scholar 

  191. Ben-Ami Bartal, I., Decety, J. & Mason, P. Empathy and pro-social behavior in rats. Science 334, 1427–1430 (2011).

    Article  PubMed  Google Scholar 

  192. Ben-Ami Bartal, I., Rodgers, D. A., Bernardez Sarria, M. S., Decety, J. & Mason, P. Pro-social behavior in rats is modulated by social experience. eLife 3, e01385 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  193. Carvalheiro, J. et al. Helping behavior in rats (Rattus norvegicus) when an escape alternative is present. J. Comp. Psychol. 133, 452–462 (2019).

    Article  PubMed  Google Scholar 

  194. Frank, E. T. et al. Saving the injured: rescue behavior in the termite-hunting ant Megaponera analis. Sci. Adv. 3, e1602187 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  195. Melis, A. P., Engelmann, J. M. & Warneken, F. Correspondence: chimpanzee helping is real, not a byproduct. Nat. Commun. 9, 615 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  196. Sato, N., Tan, L., Tate, K. & Okada, M. Rats demonstrate helping behavior toward a soaked conspecific. Anim. Cogn. 18, 1039–1047 (2015).

    Article  PubMed  Google Scholar 

  197. Silva, P. R. R. et al. Are there multiple motivators for helping behavior in rats? Front. Psychol. 11, 1795 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  198. Vasconcelos, M., Hollis, K., Nowbahari, E. & Kacelnik, A. Pro-sociality without empathy. Biol. Lett. 8, 910–912 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  199. Hollis, K. L. & Nowbahari, E. Toward a behavioral ecology of rescue behavior. Evol. Psychol. 11, 147470491301100320 (2013).

    Article  Google Scholar 

  200. Ben-Ami Bartal, I. et al. Anxiolytic treatment impairs helping behavior in rats. Front. Psychol. 7, 850 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  201. Warneken, F., Hare, B., Melis, A. P., Hanus, D. & Tomasello, M. Spontaneous altruism by chimpanzees and young children. PLoS Biol. 5, e184 (2007).

    Article  PubMed  PubMed Central  Google Scholar 

  202. Melis, A. P. et al. Chimpanzees help conspecifics obtain food and non-food items. Proc. R. Soc. B 278, 1405–1413 (2011).

    Article  PubMed  Google Scholar 

  203. Yamamoto, S., Humle, T. & Tanaka, M. Chimpanzees help each other upon request. PLoS ONE 4, e7416 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  204. Yamamoto, S., Humle, T. & Tanaka, M. Chimpanzees’ flexible targeted helping based on an understanding of conspecifics’ goals. Proc. Natl Acad. Sci. USA 109, 3588–3592 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

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N.J.R. is funded by the Royal Society, the British Academy and the Leverhulme Trust.

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Melis, A.P., Raihani, N.J. The cognitive challenges of cooperation in human and nonhuman animals. Nat Rev Psychol 2, 523–536 (2023). https://doi.org/10.1038/s44159-023-00207-7

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