Unraveling the evolution of uniquely human cognition

Edited by Richard G. Klein, Stanford University, Stanford, CA, and approved January 7, 2016 (received for review November 12, 2015)
June 6, 2016
113 (23) 6348-6354


A satisfactory account of human cognitive evolution will explain not only the psychological mechanisms that make our species unique, but also how, when, and why these traits evolved. To date, researchers have made substantial progress toward defining uniquely human aspects of cognition, but considerably less effort has been devoted to questions about the evolutionary processes through which these traits have arisen. In this article, I aim to link these complementary aims by synthesizing recent advances in our understanding of what makes human cognition unique, with theory and data regarding the processes of cognitive evolution. I review evidence that uniquely human cognition depends on synergism between both representational and motivational factors and is unlikely to be accounted for by changes to any singular cognitive system. I argue that, whereas no nonhuman animal possesses the full constellation of traits that define the human mind, homologies and analogies of critical aspects of human psychology can be found in diverse nonhuman taxa. I suggest that phylogenetic approaches to the study of animal cognition—which can address questions about the selective pressures and proximate mechanisms driving cognitive change—have the potential to yield important insights regarding the processes through which the human cognitive phenotype evolved.

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I thank B. Hare, J. Tan, C. Krupenye, and two anonymous reviewers for helpful comments on an earlier draft of this manuscript, J. Tan for sharing the photograph in Fig. 1, and the Stanton Foundation for financial support during the time the manuscript was written.


N Tinbergen, On aims and methods of ethology. Z Tierpsychol 20, 410–433 (1963).
EL MacLean, et al., How does cognition evolve? Phylogenetic comparative psychology. Anim Cogn 15, 223–238 (2012).
M Tomasello, AC Kruger, HH Ratner, Cultural learning. Behav Brain Sci 16, 495–511 (1993).
M Tomasello, H Rakoczy, What makes human cognition unique? From individual to shared to collective intentionality. Mind Lang 18, 121–147 (2003).
CD Frith, U Frith, Mechanisms of social cognition. Annu Rev Psychol 63, 287–313 (2012).
M Tomasello The Cultural Origins of Human Cognition (Harvard Univ Press, Cambridge, MA, 1999).
M Carpenter, K Nagell, M Tomasello, Social cognition, joint attention, and communicative competence from 9 to 15 months of age. Monogr Soc Res Child Dev 63, i–vi, 1–143 (1998).
R Brooks, AN Meltzoff, The development of gaze following and its relation to language. Dev Sci 8, 535–543 (2005).
N Akhtar, M Carpenter, M Tomasello, The role of discourse novelty in early word learning. Child Dev 67, 635–645 (1996).
T Callaghan, et al., Early social cognition in three cultural contexts. Monogr Soc Res Child Dev 76, 1–142 (2011).
A Shahaeian, CC Peterson, V Slaughter, HM Wellman, Culture and the sequence of steps in theory of mind development. Dev Psychol 47, 1239–1247 (2011).
D Gentner Language in Mind: Advances in the Study of Language and Thought (MIT Press, Cambridge, MA, 2003).
A Clark, Language, embodiment, and the cognitive niche. Trends Cogn Sci 10, 370–374 (2006).
DC Penn, KJ Holyoak, DJ Povinelli, Darwin’s mistake: Explaining the discontinuity between human and nonhuman minds. Behav Brain Sci 31, 109–130, discussion 130–178 (2008).
L Vygotsky, E Hanfmann, G Vakar Thought and Language (MIT Press, Cambridge, MA, 2012).
M Tomasello, J Call Primate Cognition (Oxford Univ Press, New York, 1997).
DL Cheney, RM Seyfarth How Monkeys See the World: Inside the Mind of Another Species (Univ of Chicago Press, Chicago, 1990).
DC Penn, DJ Povinelli, On the lack of evidence that non-human animals possess anything remotely resembling a ‘theory of mind’. Philos Trans R Soc Lond B Biol Sci 362, 731–744 (2007).
J Call, M Tomasello, Does the chimpanzee have a theory of mind? 30 years later. Trends Cogn Sci 12, 187–192 (2008).
B Hare, J Call, M Tomasello, Do chimpanzees know what conspecifics know? Anim Behav 61, 139–151 (2001).
B Hare, J Call, B Agnetta, M Tomasello, Chimpanzees know what conspecifics do and do not see. Anim Behav 59, 771–785 (2000).
JM Dally, NJ Emery, NS Clayton, Food-caching western scrub-jays keep track of who was watching when. Science 312, 1662–1665 (2006).
JI Flombaum, LR Santos, Rhesus monkeys attribute perceptions to others. Curr Biol 15, 447–452 (2005).
AA Sandel, E MacLean, B Hare, Evidence from four lemur species that ringtailed lemur social cognition converges with that of haplorhine primates. Anim Behav 81, 925–931 (2011).
, eds RW Byrne, A Whiten (Clarendon Press, Oxford Machiavellian Intelligence: Social Expertise and the Evolution of Intellect in Monkeys, Apes, and Humans, 1988).
, eds A Whiten, RW Byrne (Cambridge Univ Press, Cambridge, UK Machiavellian Intelligence II: Extensions and Evaluations, 1997).
M Tomasello, M Carpenter, J Call, T Behne, H Moll, Understanding and sharing intentions: The origins of cultural cognition. Behav Brain Sci 28, 675–691, discussion 691–735 (2005).
EL MacLean, B Hare, Bonobos and chimpanzees infer the target of another’s attention. Anim Behav 83, 345–353 (2012).
M Tomasello, M Carpenter, U Liszkowski, A new look at infant pointing. Child Dev 78, 705–722 (2007).
DA Leavens, WD Hopkins, Intentional communication by chimpanzees: A cross-sectional study of the use of referential gestures. Dev Psychol 34, 813–822 (1998).
F Warneken, Precocious prosociality: Why do young children help? Child Dev Perspect 9, 1–6 (2015).
H Moll, M Tomasello, Cooperation and human cognition: The Vygotskian intelligence hypothesis. Philos Trans R Soc Lond B Biol Sci 362, 639–648 (2007).
R Tuomela The Importance of Us: A Philosophical Study of Basic Social Notions (Stanford Univ Press, Stanford, CA, 1995).
M Tomasello A Natural History of Human Thinking (Harvard Univ Press, Cambridge, MA, 2014).
FBM de Waal, F Lanting Bonobo: The Forgotten Ape (Univ of California Press, Berkeley, CA, 1997).
AL Zihlman, JE Cronin, DL Cramer, VM Sarich, Pygmy chimpanzee as a possible prototype for the common ancestor of humans, chimpanzees and gorillas. Nature 275, 744–746 (1978).
R Wrangham, D Pilbeam, African apes as time machines. All Apes Great and Small, eds B Galdikas, N Briggs, L Sheeran, G Shapiro, J Goodall (Kluwer, New York), pp. 5–18 (2001).
K Prüfer, et al., The bonobo genome compared with the chimpanzee and human genomes. Nature 486, 527–531 (2012).
BT Shea, Paedomorphosis and neoteny in the pygmy chimpanzee. Science 222, 521–522 (1983).
B Hare, V Wobber, R Wrangham, The self-domestication hypothesis: Evolution of bonobo psychology is due to selection against aggression. Anim Behav 83, 573–585 (2012).
MN Muller, JC Mitani, Conflict and cooperation in wild chimpanzees. Adv Stud Behav 35, 275–331 (2005).
ML Wilson, et al., Lethal aggression in Pan is better explained by adaptive strategies than human impacts. Nature 513, 414–417 (2014).
IC Gilby, Meat sharing among the gombe chimpanzees: Harassment and reciprocal exchange. Anim Behav 71, 953–963 (2006).
K Hamann, F Warneken, JR Greenberg, M Tomasello, Collaboration encourages equal sharing in children but not in chimpanzees. Nature 476, 328–331 (2011).
AP Melis, B Hare, M Tomasello, Engineering cooperation in chimpanzees: Tolerance constraints on cooperation. Anim Behav 72, 275–286 (2006).
V Horner, A Whiten, E Flynn, FB de Waal, Faithful replication of foraging techniques along cultural transmission chains by chimpanzees and children. Proc Natl Acad Sci USA 103, 13878–13883 (2006).
T Furuichi, Female contributions to the peaceful nature of bonobo society. Evolutionary Anthropology: Issues. News Rev (Melb) 20, 131–142 (2011).
B Hare, AP Melis, V Woods, S Hastings, R Wrangham, Tolerance allows bonobos to outperform chimpanzees on a cooperative task. Curr Biol 17, 619–623 (2007).
AV Jaeggi, JM Stevens, CP Van Schaik, Tolerant food sharing and reciprocity is precluded by despotism among bonobos but not chimpanzees. Am J Phys Anthropol 143, 41–51 (2010).
KA Cronin, E De Groot, JM Stevens, Bonobos show limited social tolerance in a group setting: A comparison with chimpanzees and a test of the relational model. Folia Primatol (Basel) 86, 164–177 (2015).
B Hare, S Kwetuenda, Bonobos voluntarily share their own food with others. Curr Biol 20, R230–R231 (2010).
J Tan, B Hare, Bonobos share with strangers. PLoS One 8, e51922 (2013).
CD Stimpson, et al., Differential serotonergic innervation of the amygdala in bonobos and chimpanzees. Soc Cogn Affect Neurosci, 2015).
RW Wrangham, The evolution of sexuality in chimpanzees and bonobos. Hum Nat 4, 47–79 (1993).
RW Wrangham, BB Smuts, Sex differences in the behavioural ecology of chimpanzees in the Gombe National Park, Tanzania. J Reprod Fertil Suppl 1980, 13–31 (1980).
RW Wrangham, D Peterson Demonic Males: Apes and the Origins of Human Violence (Houghton Mifflin Harcourt, New York, 1997).
J Goodall, The Chimpanzees of Gombe: Patterns of Behavior. (Belknap Press of Harvard Univ Press, Cambridge, MA, 1986).
T Kano The Last Ape: Pygmy Chimpanzee Behavior and Ecology (Stanford University Press, Stanford, CA, 1992).
B Hare, M Brown, C Williamson, M Tomasello, The domestication of social cognition in dogs. Science 298, 1634–1636 (2002).
B Hare, et al., Social cognitive evolution in captive foxes is a correlated by-product of experimental domestication. Curr Biol 15, 226–230 (2005).
A Hernádi, A Kis, B Turcsán, J Topál, Man’s underground best friend: Domestic ferrets, unlike the wild forms, show evidence of dog-like social-cognitive skills. PLoS One 7, e43267 (2012).
A Miklósi, et al., A simple reason for a big difference: Wolves do not look back at humans, but dogs do. Curr Biol 13, 763–766 (2003).
B Hare, M Tomasello, Human-like social skills in dogs? Trends Cogn Sci 9, 439–444 (2005).
SW Porges, The Polyvagal Theory: Neurophysiological Foundations of Emotions, Attachment, Communication, and Self-Regulation, Norton Series on Interpersonal Neurobiology (Norton, New York). (2011).
C Darwin The Descent of Man, and Selection in Relation to Sex (Appleton, New York), pp. 2 v (1871).
JM Plavcan, CP van Schaik, Interpreting hominid behavior on the basis of sexual dimorphism. J Hum Evol 32, 345–374 (1997).
PL Reno, RS Meindl, MA McCollum, CO Lovejoy, Sexual dimorphism in Australopithecus afarensis was similar to that of modern humans. Proc Natl Acad Sci USA 100, 9404–9409 (2003).
JM Burkart, SB Hrdy, CP Van Schaik, Cooperative breeding and human cognitive evolution. Evol Anthropol 18, 175–186 (2009).
RG Klein, Anatomy, behavior, and modern human origins. J World Prehist 9, 167–198 (1995).
RL Cieri, SE Churchill, RG Franciscus, J Tan, B Hare, Craniofacial feminization, social tolerance, and the origins of behavioral modernity. Curr Anthropol 55, 419–443 (2014).
A Mazur, A Booth, Testosterone and dominance in men. Behav Brain Sci 21, 353–363, discussion 363–397 (1998).
KR Hill, BM Wood, J Baggio, AM Hurtado, RT Boyd, Hunter-gatherer inter-band interaction rates: Implications for cumulative culture. PLoS One 9, e102806 (2014).
M Derex, R Boyd, The foundations of the human cultural niche. Nat Commun 6, 8398 (2015).
A Powell, S Shennan, MG Thomas, Late Pleistocene demography and the appearance of modern human behavior. Science 324, 1298–1301 (2009).
S Baron-Cohen, RC Knickmeyer, MK Belmonte, Sex differences in the brain: Implications for explaining autism. Science 310, 819–823 (2005).
S Baron-Cohen, AM Leslie, U Frith, Does the autistic child have a “theory of mind”? Cognition 21, 37–46 (1985).
DI Miller, DF Halpern, The new science of cognitive sex differences. Trends Cogn Sci 18, 37–45 (2014).
S Baron-Cohen, The extreme male brain theory of autism. Trends Cogn Sci 6, 248–254 (2002).
L Christov-Moore, et al., Empathy: Gender effects in brain and behavior. Neurosci Biobehav Rev 46, 604–627 (2014).
B Auyeung, et al., Fetal testosterone and autistic traits. Br J Psychol 100, 1–22 (2009).
MH McIntyre, et al., Bonobos have a more human-like second-to-fourth finger length ratio (2D:4D) than chimpanzees: A hypothesized indication of lower prenatal androgens. J Hum Evol 56, 361–365 (2009).
E Herrmann, B Hare, J Call, M Tomasello, Differences in the cognitive skills of bonobos and chimpanzees. PLoS One 5, e12438 (2010).
F Kano, S Hirata, J Call, Social attention in the two species of pan: Bonobos make more eye contact than chimpanzees. PLoS One 10, e0129684 (2015).
E Palagi, G Cordoni, The right time to happen: Play developmental divergence in the two pan species. PLoS One 7, e52767 (2012).
AG Rosati, B Hare, Chimpanzees and bonobos exhibit divergent spatial memory development. Dev Sci 15, 840–853 (2012).
JK Rilling, et al., Differences between chimpanzees and bonobos in neural systems supporting social cognition. Soc Cogn Affect Neurosci 7, 369–379 (2012).
EL MacLean, et al., The evolution of self-control. Proc Natl Acad Sci USA 111, E2140–E2148 (2014).
EL Maclean, et al., Group size predicts social but not nonsocial cognition in lemurs. PLoS One 8, e66359 (2013).
JM Burkart, et al., The evolutionary origin of human hyper-cooperation. Nat Commun 5, 4747 (2014).
SB Hrdy Mothers and Others (Harvard Univ Press, Cambridge, MA, 2009).
B Thierry, Unity in Diversity: Lessons from Macaque Societies. Evol Anthropol 16, 224–238 (2007).
CL Nunn, L Zhu, Phylogenetic prediction to identify “evolutionary singularities.”. Modern Phylogenetic Comparative Methods and Their Application in Evolutionary Biology, ed LZ Garamszegi (Springer, Berlin), pp. 481–514 (2014).
C Organ, CL Nunn, Z Machanda, RW Wrangham, Phylogenetic rate shifts in feeding time during the evolution of Homo. Proc Natl Acad Sci USA 108, 14555–14559 (2011).
S Herculano-Houzel, The remarkable, yet not extraordinary, human brain as a scaled-up primate brain and its associated cost. Proc Natl Acad Sci USA 109, 10661–10668 (2012).
S Herculano-Houzel, The human brain in numbers: A linearly scaled-up primate brain. Front Hum Neurosci 3, 31 (2009).
CL Nunn The Comparative Approach in Evolutionary Anthropology and Biology (Univ of Chicago Press, Chicago, 2011).
E Herrmann, J Call, MV Hernàndez-Lloreda, B Hare, M Tomasello, Humans have evolved specialized skills of social cognition: The cultural intelligence hypothesis. Science 317, 1360–1366 (2007).

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Proceedings of the National Academy of Sciences
Vol. 113 | No. 23
June 7, 2016
PubMed: 27274041


Submission history

Published online: June 6, 2016
Published in issue: June 7, 2016


  1. cognitive evolution
  2. human evolution
  3. comparative psychology
  4. human uniqueness
  5. cognition


I thank B. Hare, J. Tan, C. Krupenye, and two anonymous reviewers for helpful comments on an earlier draft of this manuscript, J. Tan for sharing the photograph in Fig. 1, and the Stanton Foundation for financial support during the time the manuscript was written.


This article is a PNAS Direct Submission.



Evan L. MacLean1 [email protected]
Evolutionary Anthropology, Duke University, Durham, NC 27708;
School of Anthropology, University of Arizona, Tucson, AZ 85719


Author contributions: E.L.M. wrote the paper.

Competing Interests

The author declares no conflict of interest.

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    Unraveling the evolution of uniquely human cognition
    Proceedings of the National Academy of Sciences
    • Vol. 113
    • No. 23
    • pp. 6319-6573







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