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Putting the Altruism Back into Altruism: The Evolution of Empathy
Frans B.M. de Waal
Living Links, Yerkes National Primate Research Center, and Psychology Department, Emory University, Atlanta, Georgia 30322; email: firstname.lastname@example.org
Annu. Rev. Psychol. 2008. 59:279–300 First published online as a Review in Advance on June 5, 2007 The Annual Review of Psychology is online at http://psych.annualreviews.org This article’s doi: 10.1146/annurev.psych.59.103006.093625 Copyright c 2008 by Annual Reviews. All rights reserved 0066-4308/08/0203-0279$20.00
perception-action, perspective-taking, prosocial behavior, cooperation
Evolutionary theory postulates that altruistic behavior evolved for the return-beneﬁts it bears the performer. For return-beneﬁts to play a motivational role, however, they need to be experienced by the organism. Motivational analyses should restrict themselves, therefore, to the altruistic impulse and its knowable consequences. Empathy is an ideal candidate mechanism to underlie so-called directed altruism, i.e., altruism in response to another’s pain, need, or distress. Evidence is accumulating that this mechanism is phylogenetically ancient, probably as old as mammals and birds. Perception of the emotional state of another automatically activates shared representations causing a matching emotional state in the observer. With increasing cognition, state-matching evolved into more complex forms, including concern for the other and perspective-taking. Empathy-induced altruism derives its strength from the emotional stake it offers the self in the other’s welfare. The dynamics of the empathy mechanism agree with predictions from kin selection and reciprocal altruism theory.
INTRODUCTION . . . . . . . . . . . . . . . . . ORIGIN OF EMPATHY . . . . . . . . . . . . LEVELS OF EMPATHY . . . . . . . . . . . Emotional Contagion . . . . . . . . . . . . . Sympathetic Concern . . . . . . . . . . . . . Empathic Perspective-Taking . . . . . UNDERLYING MECHANISMS . . . Perception Action Mechanism . . . . Russian Doll Model . . . . . . . . . . . . . . FROM EMPATHY TO ALTRUISM . . . . . . . . . . . . . . . . . . . . . Emotional Contagion . . . . . . . . . . . . . Sympathetic Concern . . . . . . . . . . . . . Empathic Perspective-Taking . . . . . EMPATHY AS EVOLVED PROXIMATE MECHANISM OF DIRECTED ALTRUISM . . . . . . . . CONCLUSION . . . . . . . . . . . . . . . . . . . . 280 282 282 282 283 285 286 286 287 288 288 289 289
Sympathy . . . cannot, in any sense, be regarded as a selﬁsh principle. Smith (1759, p. 317) Altruism (biological deﬁnition): behavior that increases the recipient’s ﬁtness at a cost to the performers Ultimate cause or goal: the beneﬁts an organism or its close kin derive from a behavior, hence the probable reason why the behavior was favored by natural selection Proximate cause: situation that triggers behavior and the mechanism (psychological, neural, physiological) that enables it Empathy may be uniquely well suited for bridging the gap between egoism and altruism, since it has the property of transforming another person’s misfortune into one’s own feeling of distress. Hoffman (1981a, p. 133)
Discussions of altruistic behavior tend to suffer from a lack of distinction between function and motivation. This is due to the contrasting emphasis of biologists and psychologists, with the former focusing on what a particular behavior is good for, and the latter on how it comes about. Evolutionary explanations are built around the principle that all that natural selection can work with are the effects of behavior—not the motivation behind it. This means there is only one logical starting point for evolutionary accounts, as explained by Trivers (2002, p. 6):
“You begin with the effect of behavior on actors and recipients; you deal with the problem of internal motivation, which is a secondary problem, afterward. . . . [I]f you start with motivation, you have given up the evolutionary analysis at the outset.” This is a perfectly legitimate strategy that has yielded profound insights into the evolution of altruism (e.g., Dugatkin 2006). Unfortunately, however, these insights have not come with a new terminology: Evolutionary biology persists in using motivational terms. Thus, an action is called “selﬁsh” regardless of whether or not the actor deliberately seeks beneﬁts for itself. Similarly, an action is called “altruistic” if it beneﬁts a recipient at a cost to the actor regardless of whether or not the actor intended to beneﬁt the other. The prototypical altruist is a honeybee that stings an intruder—sacriﬁcing her life to protect the hive—even though her motivation is more likely aggressive than benign. This usage of the terms “selﬁsh” and “altruistic” oftentimes conﬂicts with their vernacular meaning (Sober & Wilson 1998). The hijacking of motivational terminology by evolutionary biologists has been unhelpful for communication about motivation per se. The way to clear up the confusion is to do what Trivers did when he decided that evolutionary analyses require that effects be considered separate from motivation. Conversely, motivational analyses require us to keep motivation separate from evolutionary considerations. It is not for nothing that biologists hammer on the distinction between ultimate and proximate (Mayr 1961, Tinbergen 1963). The ultimate cause refers to why a behavior evolved over thousands of generations, which depends on its ﬁtness consequences. The proximate cause, on the other hand, refers to the immediate situation that triggers behavior, and the role of learning, physiology, and neural processes—typically the domain of psychologists. Proximate and ultimate viewpoints do inform each other, yet are not to be conﬂated. For example, primate cooperation is
Annu. Rev. Psychol. 2008.59:279-300. Downloaded from arjournals.annualreviews.org by EMORY UNIVERSITY on 01/23/08. For personal use only.
By deﬁnition.. Helpful acts for immediate self-gain are indeed common (Dugatkin 1997).Annu. since all that animals care about are return-beneﬁts (e. disinterested helping and caring in reaction to begging or distress signals or the sight of another in pain or need.org by EMORY UNIVERSITY on 01/23/08. pain..g. altruistic behavior aimed at others in need. positive consequences for the performer and/or its kin.org • The Evolution of Empathy Directed altruism: helping or comforting behavior directed at an individual in need.g. or distress Intentional altruism: the altruist deliberately seeks to beneﬁt either the other (intentionally altruistic altruism) or itself (intentionally selﬁsh altruism) Empathy-based altruism: help and care born from empathy with another Empathy: the capacity to (a) be affected by and share the emotional state of another. i. This applies to most reciprocal altruism in the animal kingdom. but the return-beneﬁts of altruistic behavior typically remain beyond the animal’s cognitive horizon.e. on the other hand. are less likely to play a role. Helping as a conditioned response reinforced by positive outcomes for the actor. adopting his or her perspective. pain. The second possibility is help based on an appreciation of how one’s own behavior will help the other. which arose to serve reproduction. altruism carries an initial cost. hence that the act will produce a net beneﬁt. Learned altruism. (b) assess the reasons for the other’s state. Dawkins 1976. Since animals are. i. Kagan 2000. This deﬁnition extends beyond what exists in many animals. which is to yield beneﬁts for all contributors. Through its effect on food-sharing. Spontaneous. Empathy-based altruism may have similar in- trinsically rewarding qualities in that it offers the actor an emotional stake in the recipient’s well-being. if any. Altruistic impulse. therefore. and (c) identify with the other.e. EO Wilson 2005). 2. and positive consequences occur only after a signiﬁcant time interval (e. Rev. misconstrues reciprocity as a motivation. 3. Once evolved. unaware of the link between sex and reproduction.. as far as we know. Cooperation and altruistic behavior are thought to have evolved to help family members and those inclined to return the favor (Hamilton 1964. For personal use only. i. its motivation becomes disconnected from its ultimate goals. below). occur so distantly in time that the organism is unlikely to connect them with the original act.e. Psychol. Intentional altruism.g. Regardless of whether this is the whole explanation or not (see Sober & DS Wilson 1998. The altruistic impulse is to be taken very seriously. The common claim that humans are the only truly altruistic species. we may call this intentionally selﬁsh altruism.. Trivers 1971).annualreviews. 2006).. Tolerance likely is a proximate mechanism that evolved to serve the ultimate goal of cooperation. they must be engaging in sex (as do humans much of the time) without progeny in mind.59:279-300. if helping the other ameliorates the helper’s internal state (see Empathy as Evolved Proximate Mechanism. Fehr & Fischbacher 2003. promoted by social tolerance. 2008. such as the oxytocin release during suckling that may underpin maternal care (Panksepp 1998). It assumes that animals engage in reciprocal exchange with a full appreciation of how it will ultimately beneﬁt them. tolerance evens out payoff distributions (de Waal & Davis 2003. i. Silk et al.e. Since the actor seeks to beneﬁt itself. Intentionally selﬁsh altruism would require the actor to explicitly expect others to return the favor. Despite the lack of evidence for such expectations in animals. or distress.. Downloaded from arjournals. One prediction could be that the help will be reciprocated.. Melis et al. making for rather poor learning conditions. the point is that ultimate accounts stress return-beneﬁts. There are three ways in which directed altruism may come about: 1. Just as sex cannot be motivated by unforeseen consequences. Inasmuch as these beneﬁts may be quite delayed. they play. altruistic behavior cannot be motivated by unforeseen payoffs. i. it is unclear what motivational role. we may call this intentionally altruistic altruism. Since the actor seeks to beneﬁt the other. 2005). behavior often assumes motivational autonomy. the recipient reciprocates) or not at all (e. because even if altruistic behavior were partially learned based on www. This becomes clear if we consider more closely what drives directed altruism. Help based on the prediction of behavioral effects. A good example is sexual behavior. Extrinsic rewards.e.. but the term “empathy” in the present review applies even if only criterion (a) is met Motivational autonomy: independence of motivation from ultimate goals 281 . they are often assumed. Some directed altruistic behavior is promoted by built-in rewards. care for dependent kin).annualreviews. however.
Emotional contagion: emotional state-matching of a subject with an object short-term intrinsic rewards or long-term extrinsic rewards. Emotional connectedness in humans is so common. Empathy may be motivationally autonomous. Some deﬁnitions of empathy stress the sharing of emotions. Even though 282 de Waal . it presupposes this impulse given that a behavior’s consequences cannot be learned without spontaneously engaging in it in the ﬁrst place. Psychol. adopting the broadest possible deﬁnition. which is so critical for healing that adult male macaques injured during attempts to enter a new group often temporarily return to their native group. where they are more likely to receive this service (Dittus & Ratnayeke 1989). Does empathy channel altruism in the direction that evolutionary theory would predict? So..59:279-300. leads one to recognize continuity between humans and other animals as well as between human adults and young children. which is essential for the regulation of social interactions. Equivalent mechanisms operate in all animals in which reproduction relies on feeding. After this. it is a secondary development. we explore the relation between empathy and altruism. As noted by Hoffman (1981b. this by no means rules out the altruistic impulse. This review seeks to restore the altruism within altruism by exploring the role of empathy in the directed altruism of humans and other animals. which goes back as far as Lipps (1903). Signaling their state through smiling and crying. and cooperation toward shared goals. even though motivation will be kept temporarily separate from evolutionary considerations. human infants urge their caregiver to come into action (Acebo & Thoman 1995. cleaning. in the end the two will meet.” The latter deﬁnitions are so top-down.” The selection pressure to evolve rapid emotional connectedness likely started in the context of parental care long before our species evolved (Eibl-Eibesfeldt 1974 . The central thesis to be argued here. We follow a bottom-up approach instead. and warming of the young. For personal use only. The fact that mammals retain distress vocalizations into adulthood hints at the continued survival value of empathyinducing signals. cognition is often critical. Zahn-Waxler & ORIGIN OF EMPATHY Empathy allows one to quickly and automatically relate to the emotional states of others. For example. Hoffman 1975. A major question is whether evolution is likely to have selected empathy as proximate mechanism to generate directed altruism. primates often lick and clean the wounds of conspeciﬁcs (Boesch 1992). LEVELS OF EMPATHY Emotional Contagion The lowest common denominator of all empathic processes is that one party is affected by another’s emotional or arousal state. it could be applied outside the rearing context and play a role in the wider network of social relationships. Bowlby 1958). starts so early in life (e. This broad perspective on empathy. In fact.g. and that it causes altruism to be dispensed in accordance with predictions from kin selection and reciprocal altruism theory. whereas other deﬁnitions stress the capacity to put oneself into the other’s “shoes.annualreviews. 2008. Rev.Perception-action mechanism (PAM): automatically and unconsciously activated neural representations of states in the subject similar to those perceived in the object Annu. including mere emotional sensitivity to others. that they disconnect empathy from its possible antecedents. but it still needs to produce—on average and in the long run—evolutionarily advantageous outcomes. is that empathy evolved in animals as the main proximate mechanism for directed altruism. Avian or mammalian parents alert to and affected by their offspring’s needs likely out-reproduced those who remained indifferent. MacLean 1985). p. then. Downloaded from arjournals. Once the empathic capacity existed. “[H]umans must be equipped biologically to function effectively in many social situations without undue reliance on cognitive processes.org by EMORY UNIVERSITY on 01/23/08. We ﬁrst consider the various levels of empathy in animals and the underlying perceptionaction mechanism (PAM) proposed by Preston & de Waal (2002a). 79). however. coordinated activity.
and temporarily inhibit conditioned behavior if it causes pain responses in others (Church 1959. i. 2008. rats and pigeons display distress in response to perceived distress in a conspeciﬁc. 1993). they exploit emotional contagion to induce maternal distress. 1994. and shows neural and physiological correlates (e.g.. Thus.Radke-Yarrow 1990).” For example. one infant’s distress spreads quickly to its peers. Emotional contagion is not always a passive process.org by EMORY UNIVERSITY on 01/23/08. there is an automatic spreading of distress (Hoffman 1975). Personal distress is not concerned. which in turn may lead the mother to change her behavior to their advantage. Parr & Hopkins 2001). on the other hand. (1964) and Masserman et al. Sympathetic concern: concern about another’s state and attempts to ameliorate this state (e. p. Sympathy is believed to involve an otheroriented.annualreviews. with the other (Batson 1991). Similarly. For personal use only. RimmKaufman & Kagan 1996) as well as a genetic substrate (Plomin et al. De Waal (1996) speaks of “cognitive empathy” when the empathic reaction includes such contextual appraisal. Preston & de Waal 2002b) that Darwin (1982 [1871. their own response to pain (Langford et al. consolation) Cognitive empathy: empathy combined with contextual appraisal and an understanding of what caused the object’s emotional state Personal distress: self-centered distress born from empathy with another’s distress Sympathetic Concern The next evolutionary step occurs when emotional contagion is combined with appraisal of the other’s situation and attempts to understand the cause of the other’s emotions. A striking nonhuman primate example is how the continued screams of a punished infant rhesus monkey will cause other infants to embrace. At the core of these processes is adoption—in whole or in part— of another’s emotional state. Adolphs et al. or even pile on top of the victim. Personal distress. Psychol.. which mimics that of the object. Evolutionary continuity between humans and apes is reﬂected in the similarity of emotional communication (Parr & Waller 2007) as well as similar changes in brain and peripheral skin temperature in response to emotionally charged images (Parr 2001. p. Sympathy is deﬁned as “an affective response that consists of feelings of sorrow or concern for a distressed or needy other (rather than sharing the emotion of the other).g. however.annualreviews. 677). therefore.e. emotional contagion (Hatﬁeld et al. Watanabe & Ono 1986). Like human children (Potegal 2000). which then seek to reduce www. 77]) already noted that “many animals certainly sympathize with each other’s distress or danger. The psychological literature distinguishes sympathy from personal distress. Miller et al. 2006). (1959) published the ﬁrst of a series of pioneering studies on the transmission of affect in rhesus macaques. highly adaptive spreading of fear that may not involve any understanding of what triggered the initial reaction. Plutchik 1987. which in their social consequences are each other’s opposites. 1993). altruistic motivation” (Eisenberg 2000. Rev. A recent experiment demonstrated that mice perceiving other mice in pain intensify Annu. Downloaded from arjournals. that it would be strange indeed if no continuity with other species existed. Perhaps the most compelling evidence for emotional contagion came from Wechkin et al. mount. Decety & Chaminade 2003a. Whether their sacriﬁce reﬂects concern for the other (see below) remains unclear. when a room full of human newborns bursts out crying because one among them started to cry.59:279-300. who found that monkeys refuse to pull a chain that delivers food to them if doing so delivers an electric shock to and triggers pain reactions in a companion.org • The Evolution of Empathy 283 . though: The object often aims to emotionally affect the subject. A ﬂock of birds taking off all at once because one among them is startled shows a reﬂex-like. These monkeys tend to terminate projected pictures of conspeciﬁcs in a fearful pose even more rapidly than negatively conditioned stimuli. as it might also be explained as avoidance of aversive vicarious arousal. (1964). such as the extremely noisy temper tantrums of young apes when they are being rejected during weaning.. makes the affected party selﬁshly seek to alleviate its own distress. Emotional responses to displays of emotion in others are so commonplace in animals (de Waal 2003.
In a study that sought to document children’s responses to family members instructed to feign sadness (sobbing). Concern for others is different in that it relies on a separation between internally and externally generated emotions. Downloaded from arjournals. p.Consolation: comforting behavior directed at a distressed party. De Waal & van Roosmalen (1979) analyzed Figure 1 Consolation is common in humans and apes. 2008. 246) reported how his bonobo. Panzee. that the scientiﬁc establishment might reject his claims: “If I were to tell of his altruistic and obviously sympathetic behavior towards Panzee I should be suspected of idealizing an ape.” Ladygina-Kohts (2001 ) noticed similar tendencies in her young home-reared chimpanzee. Prince Chim. showed comforting attempts. 46). Perhaps the best-documented example of sympathetic concern is consolation. She discovered that the only way to get him off the roof of her house (better than reward or threat of punishment) was by acting distressed. striking similarities emerged between the reactions of one-year-old children and pets. such as putting their head in the lap of the “distressed” person (Zahn-Waxler et al. their own negative arousal (de Waal 1996. Psychol. or distress (choking). Photograph by the author. who has just been defeated in a ﬁght. For personal use only. deﬁned as reassurance provided by an uninvolved bystander to one of the combatants in a previous aggressive incident (de Waal & van Roosmalen 1979). Yerkes (1925. This separation is observable in many mammals. Here a juvenile chimpanzee puts an arm around a screaming adult male.annualreviews. such as dogs and cats. 1984). p. a third party goes over to the loser of a ﬁght and gently puts an arm around his or her shoulders (Figure 1). too. Rev.org by EMORY UNIVERSITY on 01/23/08. pain (crying). showed such concern for his sickly chimpanzee companion. such as a recent victim of aggression Annu. 284 de Waal . hence by inducing concern for herself in him. The latter. For example. but virtually absent in monkeys.59:279-300.
In this view.” Menzel (1974) was the ﬁrst to investigate whether chimpanzees understand what others know.Annu. wild chimpanzees (Kutsukake & Castles 2004. which is help ﬁne-tuned to another’s speciﬁc situation and goals (de Waal 1996). and adoption of the other’s point of view.. and de Waal & Aureli (1996) included an even larger sample.e. 104). Psychol. 2006).org • The Evolution of Empathy Empathic perspective-taking: the capacity to take another’s perspective—e. Her response likely involves emotional contagion (i. O’Connell’s (1995) content analysis of hundreds of reports conﬁrms that reassurance of distressed others is typical of apes yet rare in monkeys. 2001. Hirata 2006. Subsequent studies have conﬁrmed consolation in captive apes (Cordoni et al. Hare et al. p. Shillito et al. Povinelli 1998). Mallavarapu et al. Lewis 2002). The required self-representation is hard to establish independently. Downloaded from arjournals. The consolation gap between monkeys and the Hominoidea (i. They emphasize understanding of the other. but one common avenue is to gauge reactions to a mirror. Rev. and bystanders contact victims of serious aggression more often than they contact those who had received mild aggression. show some level of perspective-taking both in their spontaneous social behavior (de Waal 1996.org by EMORY UNIVERSITY on 01/23/08. p. 2006. 2004. when de Waal & Aureli (1996) set out to apply the same observation protocol to detect consolation in monkeys. The latter here is called “empathic perspectivetaking. 2004). These studies show that bystanders contact victims of aggression more often than they contact aggressors. humans and apes) extends even to the one situation where one would most expect consolation to occur: Macaque mothers fail to comfort their own offspring after a ﬁght (Schino et al. However. 2006). largebrained birds (Seed et al. The emotional state induced in oneself by the other now needs to be attributed to the other instead of the self.” such as in one of the oldest and best-known deﬁnitions by Smith (1759. 10) “changing places in fancy with the sufferer.e. The literature on primate behavior leaves little doubt about the existence of targeted helping. of course. hardly empathy: It is so only in combination with emotional engagement. as did others (Watts et al. that this behavior actually does reduce the distressed party’s arousal.59:279-300. 2004. Palagi et al. A major manifestation of empathic perspective-taking is so-called targeted helping. Koski & Sterck 2006. Fuentes et al. For an individual to move beyond being sensitive to others toward an explicit otherorientation requires a shift in perspective. 2006. but adds assessment of the speciﬁc reason for the other’s distress and the other’s goals. For personal use only.g. empathy is a cognitive affair dependent on imagination and mental state attribution. particularly in apes (see From Empathy to Altruism. 2000). Tree bridging is a daily occurrence in orangutans. 2008. then. 2005). A heightened selfidentity allows a subject to relate to the object’s emotional state without losing sight of the actual source of this state (Hoffman 1982... hundreds of consolations in chimpanzees. It still needs to be established. setting the stage for studies of nonhuman theory-of-mind and perspective-taking. which may explain the skepticism about nonhuman empathy (Hauser 2000. Wittig & Boesch 2003). however. understanding another’s speciﬁc situation and needs separate from one’s own—combined with vicarious emotional arousal Targeted helping: help and care based on a cognitive appreciation of the other’s speciﬁc need or situation 285 .annualreviews. with mothers regularly anticipating their offspring’s needs (van Schaik 2004. Perspective-taking by itself is.annualreviews. 1998 ) and under experimental conditions (Br¨ uer a et al. 2007). www. they failed to ﬁnd any. 2005. mother apes often brieﬂy whimper themselves when they hear their offspring do so). below). After several ups and downs in the evidence. but probably not monkeys. Empathic Perspective-Taking Psychologists usually speak of empathy only when it involves perspective-taking. 2002. current consensus seems to be that apes. and human children (Fujisawa et al. A mother ape who returns to a whimpering youngster to help it from one tree to the next—by swaying her own tree toward the one the youngster is trapped in and then drape her body between both trees— goes beyond mere concern for the other.
Perspective-taking has recently been reported for species that appear to lack MSR. For personal use only. These reports concern the ﬁnding or hiding of food. Possibly. however. Gallup (1982) was the ﬁrst to propose phylogenetic coemergence. 2008. Rochat 2003). When the subject attends to the object’s state. The more similar and socially close two individuals are. Downloaded from arjournals. The relation between MSR and the development of empathic perspective-taking holds even after the data have been sta¨ tistically controlled for age (Bischof-Kohler 1991). Reiss & Marino 2001). the link between MSR and perspective-taking is relatively loose. Psychol. Rev. e Annu. below). with compelling evidence for MSR. hence not empathic perspective-taking. UNDERLYING MECHANISMS Perception Action Mechanism Preston & de Waal (2002a) propose that at the core of the empathic capacity lies a mechanism that provides an observer (the subject) with access to the subjective state of another (the object) through the subject’s own neural and bodily representations. 2006. Johnson 1992. may apply also to phylogeny. the subject’s neural representations of similar states are automatically and unconsciously activated. the animals for which we have the most striking accounts of consolation and targeted helping are dolphins and elephants (see From Empathy to Altruism. In humans. 1997. a prediction empirically supported by the contrast between monkeys and apes. bodily sharing its emotions and needs. at the temporo-parietal junction. consolation. It should be added that self-representation is unlikely to have appeared de novo in a few large-brained animals. In the future. Emery & Clayton 2001). (1992). 2005) and birds (Bugnyar & Heinrich de Waal 2005. 2003. the right inferior parietal cortex. such as the mirror neurons discovered in macaques by di Pellegrino et al. Gallup (1983) had already predicted MSR in dolphins and elephants. we may be able to address the self-other distinction more directly through neural investigation (Decety & Chaminade 2003b).and other-produced actions (Decety & Gr` zes 2006). This lets the subject get “under the skin” of the object. and that affect communication creates matching physiological states in subject and object (Dimberg 1982. according to which self-representation emerges in small incremental steps (Lewis & Brooks-Gunn 1979. Vir´ nyi a et al. Human data suggest that a similar physiological substrate underlies both observing and experiencing an emotion (Adolphs et al. 1992). Preston & de Waal’s (2002a) PAM ﬁts Damasio’s (1994) somatic marker hypothesis of emotions as well as evidence for a link at the cellular level between perception and action. and targeted helping only in apes. the coemergence hy¨ pothesis is well-supported (Bischof-Kohler 1988. Instead of adhering to an all-or-nothing division of self-representation. Apart from the great apes. which in turn may foster sympathy and helping. 2005). Ontogenetically. The framework of developmental psychologists. some animals may reach an intermediate stage similar to that of pre-MSR human infants (de Waal et al. 1990. Recent investigations of the neural basis of human empathy conﬁrm the PAM in that they report neural similarity between self-generated and vicarious emotions 286 . and these predictions have now been conﬁrmed by the mark test. the easier the subject’s identiﬁcation with the object. Zahn-Waxler et al. underpins empathy by helping distinguish between self. in which an individual needs to locate a mark on itself that it cannot see without a mirror (Plotnik et al. which enhances the subject’s matching motor and autonomic responses.org by EMORY UNIVERSITY on 01/23/08.Mirror self-recognition (MSR): recognizing that one’s own body is reﬂected in the mirror The coemergence hypothesis predicts that mirror self-recognition (MSR) and advanced expressions of empathy appear together in both development and phylogeny.59:279-300. 2000). both mammals (Kuroshima et al.annualreviews. MSR is believed to be absent in the rest of the animal kingdom (Anderson & Gallup 1999). Levenson & Reuf 1992).
2001). at least by the apes. too. Kohler 1925) as well as successful do-as-I-do experiments with human models (Custance et al. Bodily similarity—such as with members of the same gender and species—likely enhances shared representation and identiﬁcation. Rev. Novel behavior is copied. 2005). one expects correlations between both capacities. Wolpert et al. behavioral copying (“aping”) is pronounced in all of the primates. Psychol.Annu. Without emotional engagement induced by state-matching. such as seen in the apes (Horner & Whiten 2005). even if presented so brieﬂy that they cannot be consciously perceived (Dimberg et al. Accounts of empathy as a cognitive process often neglect such automatic reactions. 2000). shared experience. such as activation of the anterior ventral insula both when we are disgusted and when we see another person expressing disgust (Wicker et al. Examples are juveniles imitating the peculiar walk of ¨ others (de Waal 1998 . and show neonatal imitation similar to that of human infants (Bard 2006. The claim is not that PAM by itself explains sympathetic concern or perspective-taking.59:279-300. 2003. 1995. If PAM is involved in both imitation and empathy. imitation. Dindo & de Waal 2006). mirror neurons ﬁre automatically to observed actions. (Carr et al. we speak of the Russian doll model. Charman et al. Because of this layered nature of the capacities involved. 2001).org • The Evolution of Empathy 287 . the motivational structure of both imitation and empathy therefore includes (a) shared representations.annualreviews.org by EMORY UNIVERSITY on 01/23/08. Other primates. Social facilitation experiments show that satiated primates begin eating again when they see others eat (Addessi & Visalberghi 2001. Paukner & Anderson 2006). Decety & Chaminade 2003a. including bodily synchronization. which has been proposed as the basis of true imitation (de Waal 1998. 2004. and www. but that it underpins these cognitively more advanced forms of empathy. 2008. which are far too rapid to be under voluntary control. 2005). 2004). empathy is a rapid routine. such as contagious yawning. with simple mechanisms at its core and more complex mechanisms and perspective-taking abilities as its outer layers. de Waal 2005). Russian Doll Model Empathy covers all the ways in which one individual’s emotional state affects another’s. In fact. This means that the Russian Doll also relates to doing as others do. even intentions (Fogassi et al. Accordingly. For personal use only. too. Functional magnetic resonance imaging studies neurally connect motor mimicry. so that we may assume PAM to underlie not only emotional state matching but also motor mimicry. in which higher cognitive levels of empathy build upon a ﬁrm. The idea that perception and action share representations is anything but new. Ferrari et al. (b) identiﬁcation with others based on physical similarity. and emulation (Figure 2). The tendency of nonhuman primates to copy each other is as spontaneous as the empathic response. In accordance with the PAM (Preston & de Waal 2002a). 2003). and social closeness. 2004. Thus. scratch themselves when others scratch themselves (Nakayama 2004). coordination. perspective-taking would be a cold phenomenon that could just as easily lead to torture as to helping (Deacon 1997. and monkeys require no extrinsic rewards to copy each other’s behavior (Bonnie & de Waal 2006). MyowaYamakoshi & Matsuzawa 1999). Downloaded from arjournals. 1997).annualreviews. Highly empathic persons are indeed more inclined to unconscious mimicry (Chartrand & Bargh 1999) and humans with autism spectrum disorder are not only deﬁcient in empathy but also imitation (Charman 2002. and serves to motivate behavioral outcomes. Perception-action mechanisms are well known for motor perception (Prinz & Hommel 2002. 2006). with empathic modeling (Platek et al. Decety & Jackson 2006. Singer et al. hard-wired basis. as conﬁrmed by electromyographic studies of muscle contractions in the human face in response to pictures of facial expressions. yawn when they see conspeciﬁcs yawn (Anderson et al. de Gelder et al. such as the PAM (de Waal 2003).
or inhibit an individual from inﬂicting pain upon another because of the vicarious negative arousal induced by the other’s distress calls. sleep. Being in sync is often a matter of life or death (Boinski & Garber 2000). .Imitation Increased Self-Other Distinction True imitation. Behavioral copying. Emotional Contagion Self-centered vicarious arousal. All of this applies to the core mechanism. When animals alert others to an outside threat. but this behavior is unlikely to be motivated by empathy with the beneﬁciary. biologists may speak of altruism or cooperation. Downloaded from arjournals.annualreviews. which develop in interaction with the environment. a mother distressed by her offspring’s distress to reassure both herself and her offspring by warming or nursing them. consolation Motor mimicry PAM Emotional contagion Figure 2 The Russian doll model of empathy and imitation. forage. Coordination. Thus. Sharing the same mechanism. Imagine a group of animals in which every member was to eat. For personal use only. Psychol. such as primates. represents the oldest kind of 288 de Waal empathy. The doll’s outer layers. too. the PAM underlies motor mimicry. emulation Empathy Perspectivetaking. the doll’s imitation side (left) correlates with the empathy side. known as personal distress. FROM EMPATHY TO ALTRUISM Not all altruistic behavior requires empathy. or play independently: This would be impossible for nomadic animals. 2006). shared goals Sympathetic concern. or vocally attract others to discovered food. often produces adaptive outcomes. coordination. shared goals. Emotional contagion may lead individuals frightened by the alarm of others to hide or ﬂee. Here. such as sympathetic concern and perspective-taking. not necessarily to the more complex outer layers of the Russian doll model.59:279-300. and true imitation. 2008. A good example seems the intensiﬁed pain response of mice seeing other mice in pain (Langford et al. with at its core the perception-action mechanism (PAM). simple empathic reactions may beneﬁt both the actor and individuals close to them. Empathy (right) induces a similar emotional state in the subject and the object. Even though the doll’s outer layers depend on prefrontal functioning and an increasing self-other distinction.org by EMORY UNIVERSITY on 01/23/08. these outer layers remain connected to its inner core. Rev. build upon this hard-wired socio-affective basis. work together for immediate selfreward. (c) automaticity and spontaneity. targeted helping Annu.
213): “In some zoos. They then literally scream in each other’s arms” (de Waal 1998 . Admittedly. unless they are rescued. Thus. Although some have argued that food-sharing may not be truly altruistic because it is subject to social pressure (Gilby 2006). In short. For example. the most common empathy-based concern for others is defense against aggression. surrounded by water-ﬁled moats .Sympathetic Concern Directed altruism requires the addition of other-orientation to emotional activation. will drown if they fall into deep water. cooperation (Kappeler & van Schaik 2006). What other than high emotional arousal can reasonably explain such bravery? Note the following description of two long-time chimpanzee friends in a zoo colony: “Not only do they often act together against attackers.annualreviews. when primates bestow care on unrelated juvenile orphans (Thierry & Anderson 1986). Chimpanzees cannot swim and. but they also seek comfort and reassurance from each other. 2006). p. she goes to the other to be embraced. but grooming is a low-cost service. Empathic Perspective-Taking Evidence for altruism based on empathic perspective-taking mostly consists of striking www. chimpanzees are kept on man-made islands. the mechanism is relatively autonomous in both animals and humans. Annu.org by EMORY UNIVERSITY on 01/23/08. Empathy is the only mechanism capable of providing a unitary motivational explanation for a wide variety of situations in which assistance is dispensed according to need.59:279-300. It is hard to imagine that the chimpanzee’s extreme hydrophobia could be overcome by a cognitive gamble on future returns. p. When Kagan (2000) argued against animal empathy by claiming that a chimpanzee would never jump into a lake to save another. Downloaded from arjournals. For personal use only. Flack & de Waal (2000) replied with a quote from Goodall (1990. Koyama et al. 1997b. or when a bonobo tries to rescue an injured bird (de Waal 1997a). individuals have sometimes made heroic efforts to save companions from drowning—and were sometimes successful. hence insulated from pressure (de Waal 1997c. which probably only emotional engagement can produce. One adult male lost his life as he tried to rescue a small infant whose incompetent mother had allowed it to fall into the water. Perhaps confusingly. In nonhuman primates. Rather. such as a rich literature on support in aggressive contexts (Harcourt & de Waal 1992). She may very well be injured. When one of them has been involved in a painful conﬂict. when a female reacts to the screams of her closest associate by defending her against a dominant male. and sharing occurs even when individuals are separated by bars. chimpanzees may deliberately engage in grooming as a way of gaining future return-favors (de Waal 1998 .org • The Evolution of Empathy 289 . Despite this. and food-sharing (Feistner & Mcgrew 1989). Nissen & Crawford 1932). 67). she takes enormous risk on behalf of the other. the problem with this view is that top-ranking individuals (who have no trouble resisting pressure) are among the most generous (de Waal 1989). A male who jumps in the water must have an overwhelming immediate motivation. .annualreviews. . the begging and distress signals typical of food beggars hint at a mediating role of empathy. Exceptional urgency and extreme motivation are required because the reaction needs to be swift and actors may face bodily danger when assisting others against an attacker. with regard to primate altruism. Fortunately. empathy often reaches beyond its original evolutionary context. empathy may motivate directed altruism in primates as often visible in the similarity of facial expressions and vocalizations of both altruists and beneﬁciaries. we do not need to rely on qualitative accounts as there exists ample systematic data. Rev.” To explain such behavior on the basis of expected return-beneﬁts makes a huge cognitive leap by injecting ultimate goals into proximate decision-making (see Introduction. such as when people send money to distant tsunami victims. above). 2008. Psychol.
the keepers hosed out all rubber tires in the enclosure and hung them on a horizontal log. p. or capsize the boat (Caldwell & Caldwell 1966.59:279-300.” For great apes. Krom was interested in a tire in which water had stayed behind. and stay close to females in labor. Downloaded from arjournals.anecdotes. experiments concern low-cost altruism. a sevenyear-old Krom had taken care of as a juvenile. Unfortunately. he was familiar with the cleaning routine. They worked their tusks under her back and under her head. 73) offers a typical description of a young female. Kakowet. except Jakie. Krom accepted his present without any acknowledgment. shot by a poacher: “Teresia and Trista became frantic and knelt down and tried to lift her up. Targeted helping has been described for cetaceans since the ancient Greeks. Dolphins are said to save companions by biting through harpoon lines or by hauling them out of nets in which they were entangled. kicking and tusking her. before releasing the chimps.” A typical paradigm . anecdotes have traditionally provided productive starting points for research (debated between Kummer et al. For personal use only. 2006. One day. However. of which I cite just two striking examples: Example 1: During one winter at the Arnhem Zoo. As it turned out. Tina. and was already scooping up water with her hand when Jakie left (de Waal 1996. there exist literally hundreds of qualitative accounts of targeted helping. Krom 290 de Waal Annu. ignored by everyone. Joubert 1991). beginning with the front one. All bonobos got out except for the smallest one. and Tallulah even went off and collected a trunkful of grass and tried to stuff it into her mouth. Dolphins also support sick companions near the surface to keep them from drowning. as any sensible chimp would. followed by the second. he carefully removed it so that no water was lost. When he reached the last tire. this particular tire was at the end of the row.annualreviews. Poole 1996) and to support or lift up others too weak to stand (Hamilton-Douglas et al. Jakie approached the scene. with six or more heavy tires in front of it. who was pulled up by Kakowet himself (de Waal 1997a. 34). the keepers went to turn on the valve to reﬁll it with water when all of a sudden the old male. p. carrying it straight to his aunt. Example 2: The two-meter-deep moat in front of the old bonobo enclosure at the San Diego Zoo had been drained for cleaning. She worked in vain for over ten minutes. Whales tend to interpose themselves between a hunter’s boat and an injured conspeciﬁc. there is a scarcity of experiments on costly altruism of the kind described above. Psychol. sometimes called “otherregarding preferences. p. After so many years. 2008. Connor & Norris 1982). placing it upright in front of her. and probably unethical. Her family tried everything to rouse her. 83). pulled and pulled at the one she wanted but couldn’t remove it. several young bonobos had entered the dry moat but were unable to get out. Elephants are known to reassure distressed companions (Payne 1998.org by EMORY UNIVERSITY on 01/23/08. After having scrubbed the moat and released the apes. came to their window. to create situations in the laboratory in which primates experience intense fear or distress. The keepers provided a ladder. Without hesitation he pushed the tires one by one off the log. At one point they succeeded in lifting her into a sitting position but her body ﬂopped back down. and so on. Moss (1988. 1990 and de Waal 1991). Immediately after Krom gave up and walked away. Rev. which are admittedly open to multiple interpretations. screaming and frantically waving his arms so as to catch their attention. More often. Because it is almost impossible.
Annu. Colman et al. chimpanzees are capable of brutally killing each other (de Waal 1998 . This is because they have already identiﬁed with the on-screen characters. even when dependent on prefrontal functioning. empathic responses to another’s fear or pain are enhanced by familiarity between subject and object (Masserman et al.annualreviews. Relationship effects are also known for rodents. These effects of previous experience have recently been conﬁrmed by functional magnetic resonance imaging: Seeing the pain of a cooperative confederate activates painrelated brain areas. p.59:279-300. Downloaded from arjournals. by covering their eyes when in a movie something gruesome is about to happen. 2006). Sometimes.annualreviews. Rev. it seems only a matter of time until otherregarding preferences will be experimentally conﬁrmed. subjects empathize with a confederate’s pleasure or distress if they perceive the relationship as cooperative. This has led authors to conclude that other-regarding preferences may be uniquely human. In monkeys. inner one. Given the overwhelming observational evidence for spontaneous helping and cooperation among primates. Wrangham & Peterson 1996). yet show an antipathic response (i. For example. hence must be capable of suppressing empathic activation in relation to conspeciﬁcs. 1964. It is impossible to prove the null hypothesis. is to offer one member of a pair the option to either secure food for itself by manipulating part A of an apparatus or food for both itself and another by manipulating part B of the same apparatus. which has led Goodall (1986. yet two recent replications failed to ﬁnd the same tendency in chimpanzees ( Jensen et al. 532) to call their victims “dechimpized. Generally. One way to cognitively control empathy is to inhibit such identiﬁcation. In human studies. How self-imposed ﬁlters and contextual appraisal modulate the brain’s empathic response remains a major unresolved issue (de Vignemont & Singer 2006). EMPATHY AS EVOLVED PROXIMATE MECHANISM OF DIRECTED ALTRUISM A Russian doll is a satisfying plaything for the biologist since every outer layer encompasses an older.e. 1959). (1969) found 1 out of 4 tested macaques to be consistently other-regarding.. hence the more accurate their state-matching. the empathic response is ampliﬁed by similarity. empathy appears wholly absent. but seeing the pain of an unfair confederate activates reward-related brain areas. however. at least in men (Singer et al. Without this emotional component. retaliatory aspect corresponds with well-documented chimpanzee behavior: These apes not only www.) The PAM model predicts that the greater the similarity or familiarity of the subject and object. Humans have so little control over empathic activation that they regularly shield themselves from it. and (b) suppressed. Miller at al. in which emotional contagion is measurable between cagemates but not between strangers (Langford et al. Thus. it is hard to see why we or other animals would care. The latter. familiarity. Silk et al. the more their representations will agree. distress at seeing the other’s pleasure or pleasure at seeing the other’s distress) if they perceive the relationship as competitive (Lanzetta & Englis 1989. 2005).. that a species’ occasional violence by no means argues against it having empathic capacities—if so. social closeness.” (It is important to note. Zillmann & Cantor 1977).org • The Evolution of Empathy 291 . human empathy would be the ﬁrst to be denied. 2006). For personal use only. 2008.g. or even turned into Schadenfreude. probably has PAM-based emotion sharing at its core (Preston & de Waal 2002a). Empathy is (a) activated in relation to those with whom one has a close or positive relationship.org by EMORY UNIVERSITY on 01/23/08. 2006. and positive experience with the other (Table 1 in Preston & de Waal 2002a). This is relevant to the origin of empathy: All prosocial behavior. Psychol. e. in relation to strangers and defectors. though. the empathy mechanism is biased the way evolutionary theory would predict.
however. the beauty of the empathy-altruism connection: The mech- anism works so well because it gives individuals an emotional stake in the welfare of others. one may well ask if helping another does not boil down to helping oneself. If altruism is produced by mechanisms. CONCLUSION More than three decades ago. 2. partners do not necessarily keep careful track of who did what for whom (Clark & Mills 1979). At the e same time. 5. Since the mechanism delivers intrinsic rewards exclusively via the other. 1997. This is. Downloaded from arjournals.59:279-300. Nancy Eisenberg. There is now increasing evidence that the brain is hardwired for social connection. and Robert Trivers for constructive feedback. Empathy. Rev. friendships) that create a longlasting communal “ﬁtness interdependence” mediated by mutual empathy. 3. A truly selfish individual would have no trouble walking away from another in need. Combined with perspective-taking abilities. it is genuinely other-oriented (Wisp´ 1991). such as empathy and bonding. Without the emotional engagement brought about by empathy. and is biased against previous defectors. Instead of assuming learned expectations or calculations about future beneﬁts. this approach emphasizes a spontaneous altruistic impulse and a mediating role of the emotions. Annu. but also take revenge upon those who have previously acted against them (de Waal & Luttrell 1988). this is no reason to call empathy-based altruism selﬁsh. that produce emotional identiﬁcation with the other. ACKNOWLEDGMENTS The author is grateful to Stephanie Preston for detailed comments on an earlier draft of the manuscript and to Jean Decety. This reciprocity mechanism is commonplace in nonhuman primates (de Waal & Brosnan 2006) and has been suggested for human relations as well. empathy favors familiar individuals and previous cooperators. Empathy could well provide the main motivation making individuals who have exchanged beneﬁts in the past to continue doing so in the future. For personal use only. An evolutionarily parsimonious account (cf.annualreviews.g. Individual interests may be served by partnerships (e. 1997. and that the same empathy mechanism proposed to underlie human altruism (Batson 1991) may underlie the directed altruism of other animals. broadly deﬁned. but as Smith (1759) argued. remains responsible for the intellectual content. Consistent with kin selection and reciprocal altruism theory. 2008. Psychol. and derive psychological and health beneﬁts not only from receiving but also from giving support (Brown & Brown 2006). It is summarized in the ﬁve conclusions below: 1. biologists deliberately removed the altruism from altruism. marriages. Cialdini et al. empathy’s motivational autonomy opens the door to intentionally altruistic altruism in a few large-brained species. Hornstein 1991..reciprocate favors within positive relationships. in fact. it is unclear what could motivate the extremely costly helping behavior occasionally observed in social animals. is a phylogenetically ancient capacity. 4. There simply is no satisfactory answer to the question of how altruistic is altruism (debated among Batson et al. Krebs 1991). whereas empathic engagement hooks one into the other’s situation. 292 de Waal .org by EMORY UNIVERSITY on 01/23/08. de Waal 1999) of directed altruism assumes similar motivational processes in humans and other animals. it is futile to try to extract the self from the process. It does. A common way in which mutually beneﬁcial exchanges are achieved is through investment in long-term bonds to which both parties contribute. Within these relationships. The author.
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S. Person Perception. III p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p225 Annu. B. Lewis. Tory Higgins and Thane S. Marc G.M. Social Emotion Motives of the Human Animal: Comprehending.T. Downloaded from arjournals. Reasoning and Problem Solving Dual-Processing Accounts of Reasoning. Adil Saribay. Derek Evan Nee. Sackett and Filip Lievens p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p419 vi Contents . and Katherine Sledge Moore p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p193 Memory Relativity of Remembering: Why the Laws of Memory Vanished Henry L. Gonzalez p p p p p p p p p p p p p p p p p p p p p p p p p p p329 Social Development. Ethology. de Waal p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p279 Anxiety Disorders Social Bonds and Posttraumatic Stress Disorder Anthony Charuvastra and Maryl` ne Cloitre p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p301 e Inference. Implicit Impressions.annualreviews. Berman. and Sharing Inner States E.org by EMORY UNIVERSITY on 01/23/08.Cognitive Processes The Mind and Brain of Short-Term Memory John Jonides. and Social Cognition Jonathan St. Roediger. For personal use only. and Evolution Putting the Altruism Back into Altruism: The Evolution of Empathy Frans B. Richard L. Rev. Social Personality. 2008. Psychol. Managing. Hodgkinson and Mark P. and Implicit Theories James S. Judgment. Pittman p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p361 Cognition in Organizations Cognition in Organizations Gerard P. and Celia M. Cindy A. Uleman.59:279-300. Evans p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p255 Comparative Psychology. Social Motivation. Healey p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p387 Selection and Placement Personnel Selection Paul R. Attribution Spontaneous Inferences. Lustig.
Volumes 49–59 p p p p p p p p p p p p p p p p p p p p p p p p673 Cumulative Index of Chapter Titles. and Fabrizio Benedetti p p p p p p p p p p p p p p p p p p p p p p p p565 Children’s Social Competence in Cultural Context Xinyin Chen and Doran C. and Bennett A. Elaine A. Richard D. Rausch p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p537 Timely Topics A Comprehensive Review of the Placebo Effect: Recent Advances and Current Thought Donald D. Volumes 49–59 p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p678 Errata An online log of corrections to Annual Review of Psychology articles may be found at http://psych.annualreviews. Alison Phillips p p p p477 Annu.shtml Contents vii . and Joseph R. Robin Morris. and Jonathan D. For personal use only.org/errata. Ken Kelley. John Weinman. Psychol. Cohen p p p p p p p p p p p p p p p p p p p p p p p p p p p p p647 Indexes Cumulative Index of Contributing Authors. Scott Rick. French p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p591 Grounded Cognition Lawrence W.59:279-300. Rev. Damien G. Roberts.Education of Special Populations The Education of Dyslexic Children from Childhood to Young Adulthood Sally E. and L. Barsalou p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p617 Neuroeconomics George Loewenstein. Leventhal. 2008. Maxwell. Downloaded from arjournals. Price. Emotion Human Abilities: Emotional Intelligence John D. Shaywitz p p p p p p p p p p p p p p p p p p p p p p p p p p p451 Health Promotion and Disease Prevention Health Psychology: The Search for Pathways Between Behavior and Health Howard Leventhal. Mayer. Shaywitz.org by EMORY UNIVERSITY on 01/23/08. and Sigal G. Barsade p p p p p p p p p p p p p p p p p p p p p p p p p p p p507 Data Analysis Sample Size Planning for Statistical Power and Accuracy in Parameter Estimation Scott E. Finniss.annualreviews.
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