The Antiquity of Empathy Frans B. M. de Waal Science 336, 874 (2012); DOI: 10.1126/science.

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grooming. Clin. Indeed. Mulligan et al. Consult. bystanders at a fight go over to the loser and put an arm around his or her shoulders or provide other calming contact (Fig. P. which also has relatively small canines (Fig.” now known as posttraumatic stress disorder (PTSD). McGurk. D. S. built around motor mirroring and shared neural representations at basal levels. a 4. As indicated by both observational and experimental studies on our closest relatives. 15. stroking. and play. 2011). Bliese. it has been suggested that these apes “may approach more closely to the common ancestor of chimpanzees and man than does any living chimpanzee” (7). therefore. humans were routinely depicted as “killer apes”—in contrast to the real apes. K. Despite being as closely related to us as chimpanzees.1126/science. In child research. intermarry. D. golden monkeys. Female bonobos maintain a close social network that allows them to collectively dominate the majority of males despite the fact that females are also the migratory sex. Hunter-gatherers illustrate a robust potential for peace and cooperation. and prosocial behavior. This literature is now recognized as one-sided because it overlooked our species' capacity for cooperation. Breslau. A.org Downloaded from www. The behavioral expression of reconciliation varies. capuchins. 19. Even though evidence for individual murder goes back hundreds of thousands of years. In chimpanzees. comparable signs of warfare (such as graveyards with weapons embedded in a large number of skeletons) are lacking from before the Agricultural Revolution [about 12.org on May 7. where they engage in sex. Yerkes National Primate Research Center. the behavior of bonobos fails to support traditional violence-based scenarios of human evolution. Clin. Pinker. which were regarded as pacifists. Hoge. VOL 336 SCIENCE After the discovery that chimpanzees often kiss and embrace shortly after a fight within their group. Bonobos express the same tendency sociosexually by means 874 18 MAY 2012 www. we should willingly engage in it. probably explained by well-developed reciprocity. and socializing. neuroscience. During most of our prehistory. Data from several thousand postconflict observations in chimpanzees indicate that consolation reduces the recipient's arousal and follows the same sex difference as reported for sympathetic concern in children. upon which touching. Acknowledgments: I thank N. The Better Angels of Our Nature: Why Violence Has Declined (Viking. behavioral economics. In primatology. Both of our closest primate relatives are marked. and close-up eye-contact by the child is interpreted as a sign of sympathetic concern. such as wolves. Yet soldiers report a deep revulsion to killing and shoot at the enemy only under pressure (1). Whereas the first species is marked by xenophobia. 1). Psychol. the second is relatively peaceful and highly empathic in both behavior and brain organization. contributed to the idea that a hallmark of humanity is aggression. Expressions of empathy are common in apes and resemble those of our own species. aid among primates is sometimes ascribed largely to kinship (11). and Robert Ardrey. we were nomadic huntergatherers. who can be lethally violent during territorial encounters between communities. This is not to imply that war was absent before then. 511 (2011). Goldstein.000 years ago (2)]. and xenophobia is only weakly developed. 928 (2009). GA 30322. Westphal. Reconciliation is a common social mechanism that would be superfluous if social life were ruled entirely by dominance and competition. C. 2). Ehlers. Wegner. Far from being a recent phenomenon. 17. Castro. 2011). seeking friendly contact especially if they otherwise enjoy a mutually beneficial relationship. If there were truly a genetic basis to our participation in lethal combat. Wessely for helpful comments on previous drafts of this article. This claim has not held up. neither in captivity nor in the wild. and by extension human nature. J. M. we end up with Ardipithecus ramidus. Nature has ensured that we find fulfillment in eating. M. After these experiences. whose cultures are nowadays not particularly known for warfare (3). Psychol. McNally. ambush. nursing. 10. but its general effect is a rapid return to preexisting levels of tolerance and affiliation. A. In order to set it apart from human cooperation with nonrelatives. B. Public Interest 4. J. that animal life. Rev. but it does mean that the common assumption that our ancestors waged perpetual wars and knew peace only at “precarious interludes” (as Winston Churchill sur- A Living Links. D.4-million-year-old hominin that has been described as relatively peaceful. New York. Adler. empathy may be the main motivator of prosocial behavior. G. 7. Relationship value appears to drive post-conflict repair (10). D. In addition. A. 45 (2003). developments in psychology. The level of cooperation among nonhuman primates tends to be underappreciated.edu mised) lacks solid archaeological backing.sciencemag. Psychol. Bonanno. 16. S. and permit travel through their territories. 2013 . and S. Bryant. but more often trade with them. and many other primates. dolphins. and Department of Psychology. New York. They do occasionally raid. Winning the War on War: The Decline of Armed Conflict Worldwide (Dutton. on the basis of DNA extracted from chimpanzee feces in the wild. They are known as the “make love. the conclusion drawn from Ardipithecus' dentition that our ancestors were less war-prone than the apes is not rigorous unless the bonobo (P. Species-typical tendencies normally come with built-in rewards. Methodologies comparing postconflict observations with baseline data to determine how species members behave in the presence versus absence of previous antagonism show that primates are generally attracted to former opponents. R. however. Mancini. 77. but also for nonprimates. by high levels of nonkin cooperation. the countermovement started with research into the survival value of friendships (8) and conflict resolution (9). This reunion process has been reported for macaques. Animal empathy is best regarded as a multilayered phenomenon. Books by Konrad Lorenz. the Austrian ethologist.14. E-mail: dewaal@emory. A. numerous studies have documented “reconciliations” in nonhuman primates. haunting memories of combat were already known to the ancient Greeks. Annu. and hyenas. owing to its reduced canine teeth as compared to those of the chimpanzee (Pan troglodytes) (5). with female apes providing comfort more often than males (13). not war” primates for solving dominance issues through sexual activity (6). Bonobos sometimes mingle across territorial borders. who described Ajax's “divine madness. However. for example. W. a family member is typically instructed to feign distress or pain. is included. an American journalist. this remained the dominant theme of biological approaches to human behavior. and animal behavior have begun to question the view. A. USA. A. chimpanzees and bonobos. (2012). C. paniscus). sex. is based on unmitigated competition. de Waal The view of humans as violent war-prone apes is poorly supported by archaeological evidence and only partly supported by the behavior of our closest primate relatives. all of which are necessary for survival and reproduction. such as Sophocles. dominant until a decade ago. J. Emory University. Deadly aggression among bonobos has thus far not been observed. fter the devastations of World War II. J. Consult. Psychol. empathy. 18. Males without genetic ties make up the majority of mutually supportive partnerships (12). gorillas..1222069 PERSPECTIVE Frans B. Clin. Until well into the 1980s. The same seems to apply to bonobos. Sci. M. they often end up with substantial psychological damage. Going back farther in time.sciencemag. which means that they are largely unrelated within each community (6). Atlanta. and kill their neighbors (4). R. that develops into more advanced cognitive perspective-taking in large-brained species.

Another way of looking at empathy is as a multilayered phenomenon that starts with automatic state-matching based on motor mimicry and shared neural representations (15). such as here between two chimpanzees watching a disturbance in Whether a mouse or their group (photograph by Frans de Waal). by unconscious empathy.retain overall adaptive value. Human empathy has been described as taking the perspective of another or imagining oneself in another's position. and assist group mates in need.available for elephants and cetaceans. such as state-matching and emotional contagion (Fig. such as when human study participants mimic observed facial expressions and report corresponding emotions even though the expressions were presented too briefly for conscious perception (16). 26). showing the same sex difference needs to be exquis. of empathy-based altruism may be represented The idea that empathy translates by Frans de Waal). a female chimpanzee may react to the thetical origin of empathy would screams of her closest associate by defending her explain the observed sex differences against an aggressive male. and a better developed circuitry for inhibiting aggression (14). Studies have also demis a reflex-like transmission of fear. into altruism and helping is widely among nonhuman primates. 1. A comparison of chimpanzee and bonobo brains supports the general view of bonobos as more empathic (6). supports the idea of evolu. If we see a child fall and scrape its knee. Although empathy.criminating because she needs to based on an appreciation of the other's specific lescent male (right). and reduced canine teeth. Ardipithecus is thought to assumed for humans and has also perspective-taking that marks human altruism. with its longer arms and shorter legs (photograph situation. Contact comfort is critically important in the lives of apes. such as “targeted helping” (assistance Fig. the behavior comes with high sensitivity to others and low levels of violence. who may role remains a point of speculation.org on May 7. Apes go out of their an elephant. danger. even though their precise orphans by wild male chimpanzees.prosocial tendencies is backed by experiments tion and sensitivity to the emotional that range from demonstrating that rats give states of others ranges from rapid priority to the liberation of a trapped companion spreading of alarm through an entire over eating chocolate (24) to those showing that group to a mother ape returning to a apes are prepared to assist others even in the whimpering youngster to help it absence of incentives.is likely to be adaptive.ample. a mother way to console distressed parties. the importance of mammalian cate about danger. That empathy is rooted most systematically studied forms of cooperain bodily connections between indi. www. Increasingly. but in er and offspring or between cooperation partners. therefore. One advantage of an viduals is reflected in pain contagion empathy-based explanation is its ability to exin mice (19) and yawn contagion plain “unrepaid” altruism. including the right dorsal amygdala and right anterior insula. Reports of spontaneous assist. Social animals plication of this capacity needs to be for it to need to coordinate travel. which assess the reason for her offspring's needs). show the species' relatively long legs. This species has more gray matter in brain regions involved in the perception of distress. Two bipedal bonobos. itely in tune with indications of hunger. thus taking great risk as well as the stimulating effect of on her behalf. This type of neurons are often mentioned in this behavior is well illustrated by the adoption of context. or choose shared benefits her body between the two. We should not be surprised.other's welfare. Ardipithecus ramidus may be the closest comparison to the bonobo in terms of its overall body proportions.sciencemag. Such coalitions are among the oxytocin (18). an adult female (left) and ado. or discomfort in her young. devote years of costly care to unrelated juveniles The fact that these neurons were (23). This increased knowledge suggests that nearly the full spectrum chimpanzee.tion in primatology (22).org SCIENCE VOL 336 18 MAY 2012 875 Downloaded from www. communi. including the cognitive grasping feet. The evolution of empathy is thought to go back to mammaFig. onstrated more complex expressions of empathy whereas the mother ape is more dis. and bonobos are likewise marked by been proposed for other mammals (21). For exfers clear adaptive value. both in their spontaneous behavior (21) makes it anatomically more similar to early hominins than to the distress in order to ameliorate its and during controlled experiments (27). 2. 3). go out of their way to give from one tree to the next by draping others access to food. 2013 . ance among primates are abundant and are also Sensitivity to emotional signals con. Mirror toward nonreciprocating nonkin. Empathy automatically produces a stake in anhave been relatively peaceful.SPECIAL SECTION of genital contacts. such as between a mothdiscovered not in humans. cognitive perspective-taking is a secondary development built around more elementary mechanisms. Psychologists commonly apply this cognitively demanding explanation of empathy even if the immediacy of the response hints at simpler processes. and exclaim “ouch!” as if what happened to the child happened at the same instant to ourselves. This hypo. The first over selfish ones (25. not each and every aptionary continuity. which may map onto nested neural processing (17). that is. such as that shown in apes and humans (20).sciencemag.in this tendency as humans. monkeys.among apes. lian maternal care. we flinch. In this view. Bodily synchroniza.

The flip side of the ingroup bias in empathy is lack of empathy for the outgroup. B. 7. I will make the case that it was warfare that culled Europe’s once-motley collection of governments to produce the modern national state. U. 1427 (2011). 11. P. is itself a result of millennia of conflict between groups of ancestral humans where. J. D. e18283 (2011). which can be adopted by a single individual. O. Press. and waste of human and material resources that it brings about. C. Castellanos. e8901 (2010). e1128 (2007). S. F. Tomasello. World Archaeol. M. de Waal. H. Thorpe. T.1126/science. Preston. C. chimpanzees frequently its evolutionary antiquity. Grossman. J. D. P. 23. would become liberal and eventually democratic. . The doll's emancipated from their evolutioninner core consists of the perception-action mechanism (PAM) ary origin. F. 3. H. 104. Stanton. 18. 35. A. Acad. J. 2. M. For example. 1555 (2006). A. F. 369 (2012). de Waal. M. Melis. USA. J. Mason. U. I. Fry. 23. R. 1399 Hyde Park Road. M. Psychol. D. U.. And this. 2013 joined the yawns of their own group members but not those of unfamiliar individuals (23). 25. Acad. Built with all life forms. 7. 145 (2003). B. To apes. M. 7786 (2007). Press. L. 9. 12.S. This occurred because. Annu. Boesch. B. P. Cogn. Coalitions and Alliances in Humans and Other Animals (Oxford Univ. Science 314. Brain Sci. F.bowles@gmail. which depend on prefrontal neural functioning. Eckhardt. B. K. ethnicities. 15. Sci. Rev. H.an intrinsic reward. de Waal. J. Italy.. Sex and Friendship in Baboons (Harvard Univ. M. A.. Neurosci. Natl. B. turn from the battlefield with PTSD. T. soldiers would have no include sympathetic concern and targeted helping.sciencemag. Lovejoy. Sci. 18. B. NM 87501. 107. 5. M. J. who were always ready to. Science 334. tragedy. But conflict—both violent and civil. Acad. 86 (2000). M. On Killing: The Psychological Cost of Learning to Kill in War and Society (Back Bay Books. W. 109. people were willing to take mortal risks in pursuit of democratic and liberal values. Charles Darwin wrote. Anthropol. J. Am. yet remain Although it is true that empathy has fundamentally connected to the PAM. S. Science 316. 26. Berkeley. F. This ingroup bias makes sense from an evolutionary perspective. The Russian doll model of multilayered empathy. 1. Hare. Bonobo: The Forgotten Ape (Univ. Warneken. and University of Siena. 6. targeted helping which seeks to integrate a multitude of groups. Glowacki. Acad. Bolé. L. Natl. PLoS ONE 5. D. as is typical of xenophobia. N. Tanaka. Schindler and the guardians of Anne Frank. Humle. We know that it can be activated by outsiders.1220999 PERSPECTIVE Samuel Bowles The origins of such varied features of contemporary life as the national state and the desire to uphold generous and civic social norms are to be found in a combination of conflict between groups and attenuation of both inequalities and conflicts within groups. B.org Downloaded from www. 1999) (originally published in 1985). D. cherished values and institutions: among them democracy. Science 312. Mayr. it is an automated response inner ones. Vigilant. de Waal. E. J. Behav. K. Natl. one that it richly deserves for the suffering. M. 10. 55 (1979). 108. 25. W. Wrangham. This is not an outcome for which empathy evolved. Suchak. sympathetic and faithful members. Science 334. 16. CA. B. Nat. 5.S. 28. because it is with the members of one's own group that apes cooperate. Siena. the rule of law. Harbaugh. A. Sci. F. New York. 8. E-mail: samuel. Langergraber. Dimberg. 24. Mitani. F.sciencemag. but most show only the group. 20. F. A. 3. it poses a profound chalPerspective-taking lenge for the modern human world. Coolidge. Boesch. This explains why collective action against those benefitting from the status quo at the expense of others. de Waal. Zak. Yamamoto. 4. D. 19. Proc. Panksepp. At the same time. W. M. 13847 (2011). as well as conflict between groups governed by different norms and institutions. capacities are often Fig. It will be important to determine political indoctrination. and humans that empathy is biased toward better understand the power of empathy requires the ingroup. U. Oxford. Rilling et al. Humans report feeling good when they do good and show activation of reward-related brain 10. de Waal. figures so prominently in our capacity to adapt to changing circumstances and to harness new knowledge for human benefit. known as the “warm glow” effect. Burghart. Affect. Phys. including enearound this hard-wired socioaffective basis. Smuts. 586 (2000). Horner. Carter. not content to free ride on the sacrifices of others. Langford et al. U.A. 1 (1933). if I am right. In contrast to the adoption of a better tool or a more productive crop. Sci. 1995). 21. P. C. Science 289. Press. 5 (2012). Santa Fe. which. B. Ecol. Psychol. de Waal.A. 74 (2009). 27. the groups with large numbers of “courageous. U. B. discussion 20 (2002). R. however. C. 1967 (2006).org on May 7. A few large-brained trouble reaching beyond the inspecies show all of the doll's layers. R. Hum. de Waal. J. We do know from studies on rodents. yet once in existence. a new institution works only if most people adopt it. 1622 (2007). F. M.A. 22. even by members of a different species. Ben-Ami Bartal. with examples such as Oskar other primates. PLoS ONE 2. M.aid and defend each Santa Fe Institute. If it weren't for empathy that underlies state-matching and emotional contagion (15). van Roosmalen. F. Elmehed. e184 (2007). Boyd. A. 1997). Ahmadi. K. 1358 (2011).A. while watching the yawns investigation of its neurological basis as well as of videotaped conspecifics. B. N. de Waal. Proc. This is another lesson whether the same self-reward system extends to from World War II. M. Hanus. M. PLoS ONE 6. S.S. and a propensity to help others and to abhor injustice. Natl. empathy may be Sympathetic concern our only hope to deal with these consolation issues. The Human Potential for Peace (Oxford Univ. 2006). 59. Proc. 17. 5. Sci. 12110 (2010). B.S. PLoS Biol. J. T. Proc. 14.com C 876 onflict has a bad name. and nations. that does not allow itself to be fully suppressed by rationalizations and areas (28). New York. both within and between societies—has also been a midwife for humanity’s most VOL 336 SCIENCE 18 MAY 2012 www. Romero. 13. D. as a result of subsequent conflicts within nations. of California Press. 3588 (2012). Thunberg. Behav. such as State-matching when we empathize with a stranded emotional contagion whale and move it back into the ocean. MA. 279 (2008). V. Harcourt. Nevertheless. 1992). the doll's outer layers my lives. Campbell. The complexity reluctance to kill nor would they reof empathy grows with increasing perspective-taking capacities. I. Cambridge. 11.. M. Decety. Science 326. References 1. Sociobiol. Soc.

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