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Survival of the Friendliest: Homo sapiens Evolved via Selection for Prosociality
Abstract
The challenge of studying human cognitive evolution is identifying unique features of our intelligence while explaining the processes by which they arose. Comparisons with nonhuman apes point to our early-emerging cooperative-communicative abilities as crucial to the evolution of all forms of human cultural cognition, including language. The human self-domestication hypothesis proposes that these early-emerging social skills evolved when natural selection favored increased in-group prosociality over aggression in late human evolution. As a by-product of this selection, humans are predicted to show traits of the domestication syndrome observed in other domestic animals. In reviewing comparative, developmental, neurobiological, and paleoanthropological research, compelling evidence emerges for the predicted relationship between unique human mentalizing abilities, tolerance, and the domestication syndrome in humans. This synthesis includes a review of the first a priori test of the self-domestication hypothesis as well as predictions for future tests.
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“both dogs and domesticated foxes outperform all non-human primates in tests of cooperative communication [34].”
From Self-domestication in Homo sapiens: Insights from comparative genomics (2017) · cites this paper as [34]
In the citing paper
“Anatomically modern humans (AMHs) exhibit a suite of craniofacial and prosocial characteristics that are reminiscent of traits distinguishing domesticated species from their wild counterparts (1–3).”
From Dosage analysis of the 7q11.23 Williams region identifies BAZ1B as a major human gene patterning the modern human face and underlying self-domestication (2019) · cites this paper as [2]
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Oxytocin enhances resting-state connectivity between amygdala and medial frontal cortex
Sripada, C. S., Phan, K. L., Labuschagne, I., Welsh, R., Nathan, P. J., & Wood, A. G. (2013) · International Journal of Neuropsychopharmacology · doi:10.1017/s1461145712000533 · Cited by 197
Evolution of correlated characters
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Hominin taxic diversity: Fact or fantasy?
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Craniofacial feminization, social tolerance, and the origins of behavioral modernity
Cieri, R. L., Churchill, S. E., Franciscus, R. G., Tan, J., & Hare, B. (2014) · Current Anthropology · doi:10.1086/677209 · Cited by 195
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Craniofacial morphology of the first Americans: Pattern and process in the peopling of the New World
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Tan, J., & Hare, B. A. (2013) · PLoS ONE · doi:10.1371/journal.pone.0051922 · Cited by 194
Self-citationHuman domestication reconsidered.
Leach, H. M. (2003) · Current Anthropology · doi:10.1086/368119 · Cited by 192
The mentalizing network orchestrates the impact of parochial altruism on social norm enforcement
Baumgärtner, T., Götte, L., Gügler, R., & Fehr, E. (2011) · Human Brain Mapping · doi:10.1002/hbm.21298 · Cited by 191
Response of Dorsomedial Prefrontal Cortex Predicts Altruistic Behavior
Waytz, A. G., Zaki, J., & Mitchell, J. P. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.6193-11.2012 · Cited by 182
Prosocial development: A longitudinal study.
Eisenberg, N., Lennon, R., & Roth, K. (1983) · Developmental Psychology · doi:10.1037/0012-1649.19.6.846 · Cited by 180
Do friends help each other? Patterns of female coalition formation in wild bonobos at Wamba
Tokuyama, N., & Furuichi, T. (2016) · Animal Behaviour · doi:10.1016/j.anbehav.2016.06.021 · Cited by 180
Koike, T., Tanabe, H. C., Okazaki, S., Nakagawa, E., Sasaki, A. T., Shimada, K., Sugawara, S. K., Takahashi, H. K., Yoshihara, K., Bosch‐Bayard, J., et al. (2015) · NeuroImage · doi:10.1016/j.neuroimage.2015.09.076 · Cited by 179
Differential changes in steroid hormones before competition in bonobos and chimpanzees
Wobber, V., Hare, B., Maboto, J., Lipson, S., Wrangham, R., & Ellison, P. T. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1007411107 · Cited by 178
Self-citationBrain ontogeny and life history in Pleistocene hominins
Hublin, J.-J., Neubauer, S., & Gunz, P. (2015) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2014.0062 · Cited by 173
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Evidence for expansion of the precuneus in human evolution
Bruner, E., Preuss, T. M., Chen, X., & Rilling, J. K. (2017) · Brain Structure and Function · doi:10.1007/s00429-015-1172-y · Cited by 172
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The Mind of the chimpanzee: ecological and experimental perspectives
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Do chimpanzees reciprocate received favours?
Melis, A. P., Hare, B. A., & Tomasello, M. (2008) · Animal Behaviour · doi:10.1016/j.anbehav.2008.05.014 · Cited by 163
Self-citationDifferences between chimpanzees and bonobos in neural systems supporting social cognition
Rilling, J. K., Scholz, J., Preuss, T. M., Glasser, M. F., Errangi, B. K., & Behrens, T. E. J. (2011) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsr017 · Cited by 163
Hare, B. A., Rosati, A. G., Kaminski, J., Bräuer, J., Call, J., & Tomasello, M. (2009) · Animal Behaviour · doi:10.1016/j.anbehav.2009.06.031 · Cited by 157
Self-citationA comparison of brain gene expression levels in domesticated and wild animals
Albert, F. W., Somel, M., Carneiro, M., Aximu-Petri, A., Halbwax, M., Thalmann, O., Blanco-Aguiar, J. A., Plyusnina, I. Z., Trut, L., Villafuerte, R., et al. (2012) · PLoS Genetics · doi:10.1371/journal.pgen.1002962 · Cited by 154
Differences in the early cognitive development of children and great apes
Wobber, V., Herrmann, E., Hare, B. A., Wrangham, R. W., & Tomasello, M. (2013) · Developmental Psychobiology · doi:10.1002/dev.21125 · Cited by 151
Self-citationHerrmann, E., & Tomasello, M. (2006) · Developmental Science · doi:10.1111/j.1467-7687.2006.00519.x · Cited by 149
Social neuroscience evidence for dehumanised perception
Harris, L. T., & Fiske, S. T. (2009) · European Review of Social Psychology · doi:10.1080/10463280902954988 · Cited by 148
What Cognitive Representations Support Primate Theory of Mind?
Martin, A., & Santos, L. R. (2016) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2016.03.005 · Cited by 147
Eyes are on us, but nobody cares: are eye cues relevant for strong reciprocity?
Fehr, E., & Schneider, F. (2009) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2009.1900 · Cited by 140
Oxytocin differentially modulates eye gaze to naturalistic social signals of happiness and anger
Domes, G., Steiner, A., Porges, S. W., & Heinrichs, M. (2013) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2012.10.002 · Cited by 139
Chimpanzees coordinate in a negotiation game
Melis, A. P., Hare, B. A., & Tomasello, M. (2009) · Evolution and Human Behavior · doi:10.1016/j.evolhumbehav.2009.05.003 · Cited by 139
Self-citationReaching around barriers: the performance of the great apes and 3–5-year-old children
Vlamings, P. H. J. M., Hare, B. A., & Call, J. (2009) · Animal Cognition · doi:10.1007/s10071-009-0265-5 · Cited by 133
Self-citationChurchill, S. E. (2014) · Wiley eBooks · doi:10.1002/9781118590836 · Cited by 133
The evolution of hominin ontogenies
Zollikofer, C. P. E., & de León, M. S. P. (2009) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2009.10.012 · Cited by 131
Humans are not alone in computing how others see the world
Whiten, A. (2013) · Animal Behaviour · doi:10.1016/j.anbehav.2013.04.021 · Cited by 127
The Eyes as Windows Into Other Minds
Großmann, T. (2017) · Perspectives on Psychological Science · doi:10.1177/1745691616654457 · Cited by 127
The development of social brain functions in infancy.
Großmann, T. (2015) · Psychological Bulletin · doi:10.1037/bul0000002 · Cited by 125
Unraveling the evolution of uniquely human cognition
MacLean, E. L. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1521270113 · Cited by 124
Prosocial development: A longitudinal study.
Eisenberg, N., Lennon, R., & Roth, K. (1983) · Developmental Psychology · doi:10.1037//0012-1649.19.6.846 · Cited by 121
Social cognitive neural networks during in-group and out-group interactions
Rilling, J. K., Dagenais, J. E., Goldsmith, D. R., Glenn, A. L., & Pagnoni, G. (2008) · NeuroImage · doi:10.1016/j.neuroimage.2008.03.044 · Cited by 117
Socially Explosive Minds: The Triple Imbalance Hypothesis of Reactive Aggression
van Honk, J., Harmon‐Jones, E., Morgan, B. E., & Schutter, D. J. L. G. (2010) · Journal of Personality · doi:10.1111/j.1467-6494.2009.00609.x · Cited by 110
Breed differences in domestic dogs’ (Canis familiaris) comprehension of human communicative signals
Wobber, V., Hare, B. A., Koler‐Matznick, J., Wrangham, R. W., & Tomasello, M. (2009) · Interaction Studies Social Behaviour and Communication in Biological and Artificial Systems · doi:10.1075/is.10.2.06wob · Cited by 109
Self-citationThe blue lizard spandrel and the island syndrome
Raia, P., Guarino, F. M., Turano, M., Polese, G., Rippa, D., Carotenuto, F., Monti, D. M., Cardi, M., & Fulgione, D. (2010) · BMC Evolutionary Biology · doi:10.1186/1471-2148-10-289 · Cited by 108
Hare, B. A. (2007) · Current Directions in Psychological Science · doi:10.1111/j.1467-8721.2007.00476.x · Cited by 108
Self-citationSocial Attention in the Two Species of Pan: Bonobos Make More Eye Contact than Chimpanzees
Kano, F., Hirata, S., & Call, J. (2015) · PLoS ONE · doi:10.1371/journal.pone.0129684 · Cited by 107
Citizen Science as a New Tool in Dog Cognition Research
Stewart, L., MacLean, E. L., Ivy, D. D., Woods, V., Cohen, E. A., Rodriguez, K. E., McIntyre, M. H., Mukherjee, S., Call, J., Kaminski, J., et al. (2015) · PLoS ONE · doi:10.1371/journal.pone.0135176 · Cited by 104
Self-citationThe evolution of language from social cognition
Seyfarth, R. M., & Cheney, D. L. (2014) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2014.04.003 · Cited by 102
Observant, nonaggressive temperament predicts theory‐of‐mind development
Wellman, H. M., Lane, J. D., LaBounty, J., & Olson, S. L. (2010) · Developmental Science · doi:10.1111/j.1467-7687.2010.00977.x · Cited by 101
A comparison of temperament in nonhuman apes and human infants
Herrmann, E., Hare, B. A., Cissewski, J., & Tomasello, M. (2011) · Developmental Science · doi:10.1111/j.1467-7687.2011.01082.x · Cited by 101
Self-citationUnconscious discrimination of social cues from eye whites in infants
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Differential Prefrontal White Matter Development in Chimpanzees and Humans
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Increasing arousal enhances inhibitory control in calm but not excitable dogs
Bray, E. E., MacLean, E. L., & Hare, B. A. (2015) · Animal Cognition · doi:10.1007/s10071-015-0901-1 · Cited by 90
Self-citationWobber, V., Hare, B. A., & Wrangham, R. W. (2008) · Journal of Human Evolution · doi:10.1016/j.jhevol.2008.03.003 · Cited by 88
Self-citationBonobos and chimpanzees infer the target of another’s attention
MacLean, E. L., & Hare, B. A. (2012) · Animal Behaviour · doi:10.1016/j.anbehav.2011.10.026 · Cited by 83
Self-citationThe emotional reactivity hypothesis and cognitive evolution
Hare, B. A., & Tomasello, M. (2005) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2005.08.010 · Cited by 82
Self-citationThe Social dog: behavior and cognition
(2014) · Choice Reviews Online · doi:10.5860/choice.186934 · Cited by 81
Eat first, share later: Hadza hunter–gatherer men consume more while foraging than in central places
Berbesque, J. C., Wood, B. M., Crittenden, A. N., Mabulla, A. Z. P., & Marlowe, F. W. (2016) · Evolution and Human Behavior · doi:10.1016/j.evolhumbehav.2016.01.003 · Cited by 75
From Hominoid to Hominid Mind: What Changed and Why?
Hare, B. A. (2010) · Annual Review of Anthropology · doi:10.1146/annurev-anthro-081309-145726 · Cited by 74
Self-citationWatching eyes on potential litter can reduce littering: evidence from two field experiments
Melissa Bateson, B., Robinson, R., Abayomi-Cole, T., Greenlees, J., O'connor, A., & Nettle, D. (2015) · PeerJ · doi:10.7717/peerj.1443 · Cited by 71
Familial influences on ovulatory function in common marmosets (Callithrix jacchus)
Wendy Saltzman, A., SCHULTZ‐DARKEN, N. J., & Abbott, D. H. (1997) · American Journal of Primatology · doi:10.1002/(sici)1098-2345(1997)41:3 · Cited by 67
Reduced self-referential neural response during intergroup competition predicts competitor harm
Cikara, M., Jenkins, A. C., Dufour, N., & Saxe, R. (2014) · NeuroImage · doi:10.1016/j.neuroimage.2014.03.080 · Cited by 67
Chimpanzees and bonobos exhibit divergent spatial memory development
Rosati, A. G., & Hare, B. A. (2012) · Developmental Science · doi:10.1111/j.1467-7687.2012.01182.x · Cited by 66
Self-citationAggression—Interactions of serotonin and testosterone in healthy men and women
Kuepper, Y., Alexander, N., Osinsky, R., Mueller, E., Schmitz, A. P., Netter, P., & Hennig, J. (2009) · Behavioural Brain Research · doi:10.1016/j.bbr.2009.09.006 · Cited by 64
Agnvall, B., Katajamaa, R., Altimiras, J., & Jensen, P. (2015) · Biology Letters · doi:10.1098/rsbl.2015.0509 · Cited by 64
Chimpanzees' ( Pan troglodytes ) strategic helping in a collaborative task
Melis, A. P., & Tomasello, M. (2013) · Biology Letters · doi:10.1098/rsbl.2013.0009 · Cited by 63
Bigger Brains Led to Bigger Bodies?: The Correlated Evolution of Human Brain and Body Size
Grabowski, M. (2016) · Current Anthropology · doi:10.1086/685655 · Cited by 63
Emotional reactivity to threat modulates activity in mentalizing network during aggression
Beyer, F., Münte, T. F., Erdmann, C., & Krämer, U. M. (2013) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nst146 · Cited by 62
McIntyre, M. H., Herrmann, E., Wobber, V., Halbwax, M., Mohamba, C., de Sousa, N., Atencia, R., Cox, D., & Hare, B. A. (2009) · Journal of Human Evolution · doi:10.1016/j.jhevol.2008.12.004 · Cited by 61
Self-citationDifferential serotonergic innervation of the amygdala in bonobos and chimpanzees
Stimpson, C. D., Barger, N., Taglialatela, J. P., Gendron‐Fitzpatrick, A., Hof, P. R., Hopkins, W. D., & Sherwood, C. C. (2015) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsv128 · Cited by 60
Why What Juveniles Do Matters in the Evolution of Cooperative Breeding
Kramer, K. L. (2014) · Human Nature · doi:10.1007/s12110-013-9189-5 · Cited by 59
Human Sclera Maintains Common Characteristics with Cartilage throughout Evolution
Seko, Y., Azuma, N., Takahashi, Y., Makino, H., Morito, T., Muneta, T., Matsumoto, K., Saito, H., Sekiya, I., & Umezawa, A. (2008) · PLoS ONE · doi:10.1371/journal.pone.0003709 · Cited by 57
Uniquely human self‐control begins at school age
Herrmann, E., Misch, A., Hernández‐Lloreda, M. V., & Tomasello, M. (2014) · Developmental Science · doi:10.1111/desc.12272 · Cited by 57
Lane, J. D., Wellman, H. M., Olson, S. L., Miller, A. L., Wang, L., & Tardif, T. Z. (2012) · Developmental Psychology · doi:10.1037/a0028825 · Cited by 56
Cognitive capacities for cooking in chimpanzees
Warneken, F., & Rosati, A. G. (2015) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2015.0229 · Cited by 53
Pseudocompetition among groups increases human cooperation in a public-goods game
Burton-Chellew, M. N., & West, S. A. (2012) · Animal Behaviour · doi:10.1016/j.anbehav.2012.07.019 · Cited by 51
Plyusnina, I. Z., Oskina, I. N., & Trut, L. N. (1991) · Applied Animal Behaviour Science · doi:10.1016/s0168-1591(05)80048-6 · Cited by 49
Infant shy temperament predicts preschoolers Theory of Mind
Mink, D., Henning, A., & Aschersleben, G. (2014) · Infant Behavior and Development · doi:10.1016/j.infbeh.2013.12.001 · Cited by 48
Mayhew, J., & Gómez, J. (2015) · American Journal of Primatology · doi:10.1002/ajp.22411 · Cited by 48
Influences of Serotonin and Testosterone in Aggression and Dominance
Bernhardt, P. C. (1997) · Current Directions in Psychological Science · doi:10.1111/1467-8721.ep11512620 · Cited by 47
Spontaneous triadic engagement in bonobos (Pan paniscus) and chimpanzees (Pan troglodytes).
MacLean, E. L., & Hare, B. A. (2013) · Journal of comparative psychology · doi:10.1037/a0030935 · Cited by 47
Self-citationBonobos: Unique in Mind, Brain and Behavior
Staes, N., Eens, M., Weiß, A., & Stevens, J. M. G. (2016) · Cited by 47
Dogs hijack the human bonding pathway
MacLean, E. L., & Hare, B. A. (2015) · Science · doi:10.1126/science.aab1200 · Cited by 46
Self-citationNelson, E., Rolian, C., Cashmore, L., & Shultz, S. (2011) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2010.1740 · Cited by 46
Globularization and domestication.
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Comparing Social Skills of Children and Apes
de Waal, F. Β. Μ., Boesch, C., Horner, V., & Whiten, A. (2008) · Science · doi:10.1126/science.319.5863.569c · Cited by 41
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The Evolution of the Hominid Brain
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Gogoleva, S. S., VOLODIN, J. A., Volodina, E. V., & Trut, L. N. (2008) · Bioacoustics · doi:10.1080/09524622.2008.9753595 · Cited by 38
Bonobo but not chimpanzee infants use socio-sexual contact with peers
Woods, V. E., & Hare, B. A. (2010) · Primates · doi:10.1007/s10329-010-0229-z · Cited by 36
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“Ultimately, these abilities led to a strong preference for others who are friendly, emotionally warm, and socially safe (Hare 2017).”
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Metadata
- Authors
- Hare, B.
- Affiliations
- Duke University (US)
- Corresponding author
- Hare, Brian
- Venue
- Annual Review of Psychology
- Publisher
- Annual Reviews
- Published
- 2017-01-03
- Volume
- 68
- Issue
- 1
- Pages
- 155-186
- ISSN
- 0066-4308 (ISSN-L)
- 1545-2085
- OpenAlex
- W2531505017
- Semantic Scholar
- 85a93b497c1862a88b7313e5f5dd5d340f4f5b7f
- Cited by
- 444
- References
- 206
- Citations by year
- 2026: 32 · 2025: 40 · 2024: 29 · 2023: 68 · 2022: 51 · 2021: 61 · 2020: 74 · 2019: 30 · 2018: 40 · 2017: 18
- FWCI
- 19.40
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Annual Review of Psychology (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Social Sciences › Cultural Studies › Language and cultural evolution
- Social Sciences › Psychology › Experimental and Cognitive Psychology › Evolutionary Psychology and Human Behavior
- Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Primate Behavior and Ecology
- Keywords
- prosocial behavior, human cognitive evolution, domestication syndrome, in-group cooperation, aggression, language evolution, mentalization, tolerance, social cognition, human evolution
- MeSH terms
- Animals, Behavior, Animal, Communication, Cooperative Behavior, Biological Evolution, Humans, Intelligence, Social Behavior, Temperament
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