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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: dewaal@emory.edu
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.S9.103006.09362S
Copyright © 2008 by Annual Reviews. All rights reserved
0066-4308/08/0203-0279$20.00
Key Words
perception-action, perspective-taking, prosocial behavior, cooperation
Abstract
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.
279
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
Contents
INTRODUCTION................. 280
ORIGIN OF EMPATHY............ 282
LEVELS OF EMPATHY........... 282
Emotional Contagion............. 282
Sympathetic Concern............. 283
Empathic Perspective-Taking..... 285
UNDERLYING MECHANISMS... 286
Perception Action Mechanism .... 286
Russian Doll Model.............. 287
FROM EMPATHY TO
ALTRUISM..................... 288
Emotional Contagion............. 288
Sympathetic Concern............. 289
Empathic Perspective-Taking..... 289
EMPATHY AS EVOLVED
PROXIMATE MECHANISM OF
DIRECTED ALTRUISM........ 291
CONCLUSION.................... 292
Sympathy... cannot, in any sense, be regarded as a selfish principle.
Smith (1759, p. 317)
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)
INTRODUCTION
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.... [IJfyou 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
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de Waal
promoted by social tolerance. Through its effect on food-sharing, tolerance evens out payoff distributions (de Waal & Davis 2003, Melis et al. 2006). Tolerance likely is a proximate mechanism that evolved to serve the ultimate goal of cooperation, which is to yield benefits for all contributors.
Cooperation and altruistic behavior are thought to have evolved to help family members and those inclined to return the favor (Hamilton 1964, Trivers 1971). Regardless of whether this is the whole explanation or not (see Sober & DS Wilson 1998, EO Wilson 2005), the point is that ultimate accounts stress return-benefits, i.e., positive consequences for the performer and/or its kin. Inasmuch as these benefits may be quite delayed, however, it is unclear what motivational role, if any, they play. This becomes clear if we consider more closely what drives directed altruism, i.e., altruistic behavior aimed at others in need, pain, or distress. There are three ways in which directed altruism may come about:
1. Altruistic impulse. Spontaneous, disinterested helping and caring in reaction to begging or distress signals or the sight of another in pain or need.
2. Learned altruism. Helping as a conditioned response reinforced by positive outcomes for the actor.
3. Intentional altruism. Help based on the prediction of behavioral effects. One prediction could be that the help will be reciprocated, hence that the act will produce a net benefit. Since the actor seeks to benefit itself, we may call this intentionally selfish altruism. The second possibility is help based on an appreciation of how one's own behavior will help the other. Since the actor seeks to benefit the other, we may call this intentionally altruistic altruism.
Some directed altruistic behavior is promoted by built-in rewards, such as the oxytocin release during suckling that may underpin maternal care (Panksepp 1998). 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, i.e., if helping the other ameliorates the helper's internal state (see Empathy as Evolved Proximate Mechanism, below). Extrinsic rewards, on the other hand, are less likely to play a role. By definition, altruism carries an initial cost, and positive consequences occur only after a significant time interval (e.g., the recipient reciprocates) or not at all (e.g., care for dependent kin), making for rather poor learning conditions.
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, they are often assumed. The common claim that humans are the only truly altruistic species, since all that animals care about are return-benefits (e.g., Dawkins 1976, Fehr & Fischbacher 2003, Kagan 2000, Silk et al. 2005), misconstrues reciprocity as a motivation. It assumes that animals engage in reciprocal exchange with a full appreciation of how it will ultimately benefit them. Helpful acts for immediate self-gain are indeed common (Dugatkin 1997), but the return-benefits of altruistic behavior typically remain beyond the animal's cognitive horizon, i.e., occur so distantly in time that the organism is unlikely to connect them with the original act. This applies to most reciprocal altruism in the animal kingdom.
Once evolved, behavior often assumes motivational autonomy, i.e., its motivation becomes disconnected from its ultimate goals. A good example is sexual behavior, which arose to serve reproduction. Since animals are, as far as we know, unaware of the link between sex and reproduction, they must be engaging in sex (as do humans much of the time) without progeny in mind. Just as sex cannot be motivated by unforeseen consequences, altruistic behavior cannot be motivated by unforeseen payoffs.
The altruistic impulse is to be taken very seriously, therefore, because even if altruistic behavior were partially learned based on
Directed altruism:
helping or comforting behavior directed at an individual in need, pain, 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, (b) assess the reasons for the other's state, and (c) identify with the other, adopting his or her perspective. This definition extends beyond what exists in many animals, but the term ''empathy" in the present review applies even if only criterion (a) is met
Motivational autonomy:
independence of motivation from ultimate goals
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Perception-action mechanism (PAM):
automatically and unconsciously activated neural representations of states in the subject similar to those perceived in the object
Emotional contagion:
emotional
state-matching of a
subject with an
object
short-term intrinsic rewards or long-term extrinsic rewards, this by no means rules out the altruistic impulse. In fact, it presupposes this impulse given that a behavior's consequences cannot be learned without spontaneously engaging in it in the first place.
This review seeks to restore the altruism within altruism by exploring the role of empathy in the directed altruism of humans and other animals. Some definitions of empathy stress the sharing of emotions, whereas other definitions stress the capacity to put oneself into the other's "shoes." The latter definitions are so top-down, however, that they disconnect empathy from its possible antecedents. We follow a bottom-up approach instead, adopting the broadest possible definition, including mere emotional sensitivity to others. We first consider the various levels of empathy in animals and the underlying perception-action mechanism (PAM) proposed by Preston & de Waal (2002a). After this, we explore the relation between empathy and altruism.
A major question is whether evolution is likely to have selected empathy as proximate mechanism to generate directed altruism. Does empathy channel altruism in the direction that evolutionary theory would predict? So, even though motivation will be kept temporarily separate from evolutionary considerations, in the end the two will meet. Empathy may be motivationally autonomous, but it still needs to produce—on average and in the long run—evolutionarily advantageous outcomes. The central thesis to be argued here, then, is that empathy evolved in animals as the main proximate mechanism for directed altruism, and that it causes altruism to be dispensed in accordance with predictions from kin selection and reciprocal altruism theory.
ORIGIN OF EMPATHY
Empathy allows one to quickly and automatically relate to the emotional states of others, which is essential for the regulation of social interactions, coordinated activity, and cooperation toward shared goals. Even though
cognition is often critical, it is a secondary development. As noted by Hoffman (1981b, p. 79), "[HJumans must be equipped biologically to function effectively in many social situations without undue reliance on cognitive processes."
The selection pressure to evolve rapid emotional connectedness likely started in the context of parental care long before our species evolved (Eibl-Eibesfeldt 1974 [1971], MacLean 1985). Signaling their state through smiling and crying, human infants urge their caregiver to come into action (Acebo & Thoman 1995, Bowlby 1958). Equivalent mechanisms operate in all animals in which reproduction relies on feeding, cleaning, and warming of the young. Avian or mammalian parents alert to and affected by their offspring's needs likely out-reproduced those who remained indifferent.
Once the empathic capacity existed, it could be applied outside the rearing context and play a role in the wider network of social relationships. The fact that mammals retain distress vocalizations into adulthood hints at the continued survival value of empathy-inducing signals. For example, primates often lick and clean the wounds of conspecifics (Boesch 1992), 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 (Dittos & Ratnayeke 1989).
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. This broad perspective on empathy, which goes back as far as Lipps (1903), leads one to recognize continuity between humans and other animals as well as between human adults and young children. Emotional connectedness in humans is so common, starts so early in life (e.g., Hoffman 1975, Zahn-Waxier &
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de Waal
Radke-Yarrow 1990), and shows neural and physiological correlates (e.g., Adolphs et al. 1994, Decety & Chaminade 2003a, Rimm-Kaufman & Kagan 1996) as well as a genetic substrate (Plomin et al. 1993), that it would be strange indeed if no continuity with other species existed. 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, Parr & Hopkins 2001).
A flock of birds taking off all at once because one among them is startled shows a reflex-like, highly adaptive spreading of fear that may not involve any understanding of what triggered the initial reaction. Similarly when a room full of human newborns bursts out crying because one among them started to cry, there is an automatic spreading of distress (Hoffman 1975). At the core of these processes is adoption—in whole or in part— of another's emotional state, i.e., emotional contagion (Hatfield et al. 1993). Emotional contagion is not always a passive process, though: The object often aims to emotionally affect the subject, such as the extremely noisy temper tantrums of young apes when they are being rejected during weaning. Like human children (Potegal 2000), they exploit emotional contagion to induce maternal distress, which in turn may lead the mother to change her behavior to their advantage.
Emotional responses to displays of emotion in others are so commonplace in animals (de Waal 2003, Plutchik 1987, Preston & de Waal 2002b) that Darwin (1982 [1871, p. 77]) already noted that "many animals certainly sympathize with each other's distress or danger." For example, rats and pigeons display distress in response to perceived distress in a conspecific, and temporarily inhibit conditioned behavior if it causes pain responses in others (Church 1959, Watanabe & Ono 1986). A recent experiment demonstrated that mice perceiving other mice in pain intensify
their own response to pain (Langford et al. 2006).
Miller et al. (1959) published the first of a series of pioneering studies on the transmission of affect in rhesus macaques. These monkeys tend to terminate projected pictures of conspecifics in a fearful pose even more rapidly than negatively conditioned stimuli. Perhaps the most compelling evidence for emotional contagion came from Wechkin et al. (1964) and Masserman et al. (1964), 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. Whether their sacrifice reflects concern for the other (see below) remains unclear, however, as it might also be explained as avoidance of aversive vicarious arousal.
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. De Waal (1996) speaks of "cognitive empathy" when the empathic reaction includes such contextual appraisal.
The psychological literature distinguishes sympathy from personal distress, which in their social consequences are each other's op-posites. 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). Sympathy is believed to involve an other-oriented, altruistic motivation" (Eisenberg 2000, p. 677). Personal distress, on the other hand, makes the affected party selfishly seek to alleviate its own distress, which mimics that of the object. Personal distress is not concerned, therefore, with the other (Batson 1991). A striking nonhuman primate example is how the continued screams of a punished infant rhesus monkey will cause other infants to embrace, mount, or even pile on top of the victim. Thus, one infant's distress spreads quickly to its peers, which then seek to reduce
Sympathetic concern: concern about another's state and attempts to ameliorate this state (e.g., 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
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28)
Consolation:
comforting behavior directed at a distressed party, such as a recent victim of aggression
their own negative arousal (de Waal 1996, p. 46).
Concern for others is different in that it relies on a separation between internally and externally generated emotions. This separation is observable in many mammals. In a study that sought to document children's responses to family members instructed to feign sadness (sobbing), pain (crying), or distress (choking), striking similarities emerged between the reactions of one-year-old children and pets, such as dogs and cats. The latter, too, showed comforting attempts, such as putting their head in the lap of the "distressed" person (Zahn-Waxler etal. 1984).
Yerkes (1925, p. 246) reported how his bonobo, Prince Chim, showed such concern for his sickly chimpanzee companion, 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 [1935]) noticed similar tendencies in her young home-reared chimpanzee. 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, hence by inducing concern for herself in him.
Perhaps the best-documented example of sympathetic concern is consolation, defined as reassurance provided by an uninvolved bystander to one of the combatants in a previous aggressive incident (de Waal & van Roosmalen 1979). For example, a third party goes over to the loser of a fight and gently puts an arm around his or her shoulders (Figure 1). De Waal & van Roosmalen (1979) analyzed
Figure 1
Consolation is common in humans and apes, but virtually absent in monkeys. Here a juvenile
chimpanzee puts an arm around a screaming adult male, who has just been defeated in a fight. Photograph by the author.
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de Waal
hundreds of consolations in chimpanzees, and de Waal & Aureli (1996) included an even larger sample. These studies show that bystanders contact victims of aggression more often than they contact aggressors, and bystanders contact victims of serious aggression more often than they contact those who had received mild aggression.
Subsequent studies have confirmed consolation in captive apes (Cordoni et al. 2004; Fuentes et al. 2002; Koski & Sterck 2006; Mallavarapu et al. 2006; Palagi et al. 2004, 2006), wild chimpanzees (Kutsukake & Castles 2004, Wittig & Boesch 2003), large-brained birds (Seed et al. 2007), and human children (Fujisawa et al. 2006). However, when de Waal & Aureli (1996) set out to apply the same observation protocol to detect consolation in monkeys, they failed to find any, as did others (Watts et al. 2000). The consolation gap between monkeys and the Hominoidea (i.e., 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. 2004). O'ConnelFs (1995) content analysis of hundreds of reports confirms that reassurance of distressed others is typical of apes yet rare in monkeys. It still needs to be established, however, that this behavior actually does reduce the distressed party's arousal.
Empathic Perspective-Taking
Psychologists usually speak of empathy only when it involves perspective-taking. They emphasize understanding of the other, and adoption of the other's point of view. In this view, then, empathy is a cognitive affair dependent on imagination and mental state attribution, which may explain the skepticism aboutnonhuman empathy (Hauser 2000, Povinelli 1998). Perspective-taking by itself is, of course, hardly empathy: It is so only in combination with emotional engagement. The latter here is called "empathic perspective-taking,"  such  as  in  one  of the oldest
and best-known definitions by Smith (1759, p. 10) "changing places in fancy with the sufferer."
Menzel (1974) was the first to investigate whether chimpanzees understand what others know, setting the stage for studies of nonhu-man theoiy-of-mind and perspective-taking. After several ups and downs in the evidence, current consensus seems to be that apes, but probably not monkeys, show some level of perspective-taking both in their spontaneous social behavior (de Waal 1996, 1998 [1982]) and under experimental conditions (Brauer et al. 2005; Hare et al. 2001, 2006; Hirata 2006; Shillito et al. 2005).
A major manifestation of empathic perspective-taking is so-called targeted helping, which is help fine-tuned to another's specific situation and goals (de Waal 1996). The literature on primate behavior leaves little doubt about the existence of targeted helping, particularly in apes (see From Empathy to Altruism, below). 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. Her response likely involves emotional contagion (i.e., mother apes often briefly whimper themselves when they hear their offspring do so), but adds assessment of the specific reason for the other's distress and the other's goals. Tree bridging is a daily occurrence in orangutans, with mothers regularly anticipating their offspring's needs (van Schaik2004, p. 104).
For an individual to move beyond being sensitive to others toward an explicit other-orientation requires a shift in perspective. The emotional state induced in oneself by the other now needs to be attributed to the other instead of the self. A heightened self-identity allows a subj ect to relate to the obj ect's emotional state without losing sight of the actual source of this state (Hoffman 1982, Lewis 2002). The required self-representation is hard to establish independently, but one common avenue is to gauge reactions to a mirror.
Empathic
perspective-taking:
the capacity to take another's
perspective—e.g., 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
TVTinv.annualrevieTvs.org • The Evolution of Empathy
Mirror
self-recognition (MSR): recognizing that one's own body is reflected in the
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The coemergence hypothesis predicts that mirror self-recognition (MSR) and advanced expressions of empathy appear together in both development and phylogeny.
Ontogenetically, the coemergence hypothesis is well-supported (Bischof-Köhler 1988, Johnson 1992, Zahn-Waxler et al. 1992). The relation between MSR and the development of empathic perspective-taking holds even after the data have been statistically controlled for age (Bischof-Köhler 1991). Gallup (1982) was the first to propose phylogenetic coemergence, a prediction empirically supported by the contrast between monkeys and apes, with compelling evidence for MSR, consolation, and targeted helping only in apes.
Apart from the great apes, the animals for which we have the most striking accounts of consolation and targeted helping are dolphins and elephants (see From Empathy to Altruism, below). Gallup (1983) had already predicted MSR in dolphins and elephants, and these predictions have now been confirmed by the mark test, in which an individual needs to locate a mark on itself that it cannot see without a mirror (Plotnik et al. 2006, Reiss & Marino 2001). MSR is believed to be absent in the rest of the animal kingdom (Anderson & Gallup 1999).
It should be added that self-representation is unlikely to have appeared de novo in a few large-brained animals. The framework of developmental psychologists, according to which self-representation emerges in small incremental steps (Lewis & Brooks-Gunn 1979, Rochat 2003), may apply also to phylogeny. Instead of adhering to an all-or-nothing division of self-representation, some animals may reach an intermediate stage similar to that of pre-MSR human infants (de Waal et al. 2005).
Possibly, the link between MSR and perspective-taking is relatively loose. Perspective-taking has recently been reported for species that appear to lack MSR, both mammals (Kuroshima et al. 2003, Viranyi et al. 2005) and birds (Bugnyar & Heinrich
2005, Emery & Clayton 2001). These reports concern the finding or hiding of food, however, hence not empathic perspective-taking. In the future, we may be able to address the self-other distinction more directly through neural investigation (Decety & Chaminade 2003b). In humans, the right inferior parietal cortex, at the temporo-parietal junction, underpins empathy by helping distinguish between self- and other-produced actions (Decety & Grezes 2006).
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. When the subject attends to the object's state, the subject's neural representations of similar states are automatically and unconsciously activated. The more similar and socially close two individuals are, the easier the subject's identification with the object, which enhances the subject's matching motor and autonomic responses. This lets the subject get "under the skin" of the object, bodily sharing its emotions and needs, which in turn may foster sympathy and helping. Preston & de Waal's (2002 a) 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, such as the mirror neurons discovered in macaques by di Pellegrino et al. (1992).
Human data suggest that a similar physiological substrate underlies both observing and experiencing an emotion (Adolphs et al. 1997, 2000), and that affect communication creates matching physiological states in subject and object (Dimberg 1982, 1990; Levenson & Reuf 1992). Recent investigations of the neural basis of human empathy confirm the PAM in that they report neural similarity between self-generated and vicarious emotions
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de Waal
(Carr etal. 2003, Decety& Chaminade 2003a, Decety & Jackson 2006, de Gelder et al. 2004, Singer et al. 2004), such as activation of the anterior ventral insula both when we are disgusted and when we see another person expressing disgust (Wicker et al. 2003).
The idea that perception and action share representations is anything but new. Accordingly, empathy is a rapid routine, as confirmed by electromyographic studies of muscle contractions in the human face in response to pictures of facial expressions, even if presented so briefly that they cannot be consciously perceived (Dimberg et al. 2000). Accounts of empathy as a cognitive process often neglect such automatic reactions, which are far too rapid to be under voluntary control.
Russian Doll Model
Empathy covers all the ways in which one individual's emotional state affects another's, with simple mechanisms at its core and more complex mechanisms and perspective-taking abilities as its outer layers. Because of this layered nature of the capacities involved, we speak of the Russian doll model, in which higher cognitive levels of empathy build upon a firm, hard-wired basis, such as the PAM (de Waal 2003). The claim is not that PAM by itself explains sympathetic concern or perspective-taking, but that it underpins these cognitively more advanced forms of empathy, and serves to motivate behavioral outcomes. Without emotional engagement induced by state-matching, perspective-taking would be a cold phenomenon that could just as easily lead to torture as to helping (Deacon 1997, de Waal 2005).
Perception-action mechanisms are well known for motor perception (Prinz & Hommel 2002, Wolpert et al. 2001), so that we may assume PAM to underlie not only emotional state matching but also motor mimicry. This means that the Russian Doll also relates to doing as others do, including bodily synchronization, coordination, imitation, and emulation (Figure 2). If PAM is
involved in both imitation and empathy, one expects correlations between both capacities. 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, Charman et al. 1997). Functional magnetic resonance imaging studies neurally connect motor mimicry, such as contagious yawning, with empathic modeling (Platek et al. 2005).
Other primates, too, yawn when they see conspecifics yawn (Anderson et al. 2004, Paukner & Anderson 2006). In fact, behavioral copying ("aping") is pronounced in all of the primates. Social facilitation experiments show that satiated primates begin eating again when they see others eat (Addessi & Visalberghi 2001, Dindo & de Waal 2006), scratch themselves when others scratch themselves (Nakayama 2004), and show neonatal imitation similar to that of human infants (Bard 2006, Ferrari et al. 2006). Novel behavior is copied, too, at least by the apes. Examples are juveniles imitating the peculiar walk of others (de Waal 1998 [1982], Köhler 1925) as well as successful do-as-I-do experiments with human models (Custance et al. 1995, Myowa-Yamakoshi & Matsuzawa 1999).
Bodily similarity—such as with members of the same gender and species—likely enhances shared representation and identification, which has been proposed as the basis of true imitation (de Waal 1998, 2001), such as seen in the apes (Horner & Whiten 2005). The tendency of nonhuman primates to copy each other is as spontaneous as the empathic response. Thus, mirror neurons fire automatically to observed actions, even intentions (Fogassi et al. 2005), and monkeys require no extrinsic rewards to copy each other's behavior (Bonnie & de Waal 2006).
In accordance with the PAM (Preston & de Waal 2002a), the motivational structure of both imitation and empathy therefore includes (a) shared representations; (b) identification with others based on physical similarity, shared experience, and social closeness; and
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Imitation
True imitation, emulation «
Coordination, shared goals
Motor mimicry
^^^^^^^^
Empathy
Perspective-taking, targeted helping
Sympathetic
concern,
consolation
)-
Emotional contagion
Figure 2
The Russian doll model of empathy and imitation. Empathy (right) induces a similar emotional state in the subject and the object, with at its core the perception-action mechanism (PAM). The doll's outer layers, such as sympathetic concern and perspective-taking, build upon this hard-wired socio-affective basis. Sharing the same mechanism, the doll's imitation side (left) correlates with the empathy side. Here, the PAM underlies motor mimicry, coordination, shared goals, and true imitation. Even though the doll's outer layers depend on prefrontal functioning and an increasing self-other distinction, these outer layers remain connected to its inner core.
(f) automaticity and spontaneity. All of this applies to the core mechanism, not necessarily to the more complex outer layers of the Russian doll model, which develop in interaction with the environment.
FROM EMPATHY TO ALTRUISM
Not all altruistic behavior requires empathy. When animals alert others to an outside threat, work together for immediate self-reward, or vocally attract others to discovered food, biologists may speak of altruism or cooperation, but this behavior is unlikely to be motivated by empathy with the beneficiary.
Emotional Contagion
Self-centered vicarious arousal, known as personal distress, represents the oldest kind of
empathy. A good example seems the intensified pain response of mice seeing other mice in pain (Langford et al. 2006). Emotional contagion may lead individuals frightened by the alarm of others to hide or flee, a mother distressed by her offspring's distress to reassure both herself and her offspring by warming or nursing them, or inhibit an individual from inflicting pain upon another because of the vicarious negative arousal induced by the other's distress calls. Thus, simple empathic reactions may benefit both the actor and individuals close to them.
Behavioral copying, too, often produces adaptive outcomes. Imagine a group of animals in which every member was to eat, sleep, forage, or play independently: This would be impossible for nomadic animals, such as primates. Being in sync is often a matter of life or death (Boinski & Garber 2000).
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Sympathetic Concern
Directed altruism requires the addition of other-orientation to emotional activation. In nonhuman primates, the most common empathy-based concern for others is defense against aggression. 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. For example, when a female reacts to the screams of her closest associate by defending her against a dominant male, she takes enormous risk on behalf of the other. She may very well be injured. 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, but they also seek comfort and reassurance from each other. When one of them has been involved in a painful conflict, she goes to the other to be embraced. They then literally scream in each other's arms" (de Waal 1998 [1982], p. 67).
When Kagan (2000) argued against animal empathy by claiming that a chimpanzee would never jump into a lake to save another, Flack & de Waal (2000) replied with a quote from Goodall (1990, p. 213): "In some zoos, chimpanzees are kept on man-made islands, surrounded by water-filed moats... Chimpanzees cannot swim and, unless they are rescued, will drown if they fall into deep water. Despite this, individuals have sometimes made heroic efforts to save companions from drowning—and were sometimes successful. 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."
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, above). Admittedly, chimpanzees may deliberately engage in grooming as a way of gaining future return-favors (de Waal 1998 [1982], 1997b; Koyama et al. 2006), but grooming is
a low-cost service. It is hard to imagine that the chimpanzee's extreme hydrophobia could be overcome by a cognitive gamble on future returns. A male who jumps in the water must have an overwhelming immediate motivation, which probably only emotional engagement can produce.
Fortunately, with regard to primate altruism, we do not need to rely on qualitative accounts as there exists ample systematic data, such as a rich literature on support in aggressive contexts (Harcourt & de Waal 1992), cooperation (Kappeler & van Schaik 2006), and food-sharing (Feistner & Mcgrew 1989). Although some have argued that food-sharing may not be truly altruistic because it is subject to social pressure (Gilby 2006), the problem with this view is that top-ranking individuals (who have no trouble resisting pressure) are among the most generous (de Waal 1989), and sharing occurs even when individuals are separated by bars, hence insulated from pressure (de Waal 1997c, Nissen & Crawford 1932). Rather, the begging and distress signals typical of food beggars hint at a mediating role of empathy.
In short, empathy may motivate directed altruism in primates as often visible in the similarity of facial expressions and vocalizations of both altruists and beneficiaries. 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. Perhaps confusingly, the mechanism is relatively autonomous in both animals and humans. Thus, empathy often reaches beyond its original evolutionary context, such as when people send money to distant tsunami victims, when primates bestow care on unrelated juvenile orphans (Thierry & Anderson 1986), or when a bonobo tries to rescue an injured bird (de Waal 1997a).
Empathic Perspective-Taking
Evidence for altruism based on empathic perspective-taking mostly consists of striking
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anecdotes, which are admittedly open to multiple interpretations. However, anecdotes have traditionally provided productive starting points for research (debated between Kummer et al. 1990 and de Waal 1991).
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. Dolphins also support sick companions near the surface to keep them from drowning, and stay close to females in labor. Whales tend to interpose themselves between a hunter's boat and an injured conspecific, or capsize the boat (Caldwell & Caldwell 1966, Connor & Norris 1982).
Elephants are known to reassure distressed companions (Payne 1998, Poole 1996) and to support or lift up others too weak to stand (Hamilton-Douglas etal. 2006, Joubert 1991). Moss (1988, p. 73) offers a typical description of a young female, Tina, shot by a poacher: "Teresia and Trista became frantic and knelt down and tried to lift her up. They worked their tusks under her back and under her head. At one point they succeeded in lifting her into a sitting position but her body flopped back down. Her family tried everything to rouse her, kicking and tusking her, and Tallulah even went off and collected a trunkful of grass and tried to stuff it into her mouth."
For great apes, there exist literally hundreds of qualitative accounts of targeted helping, of which I cite just two striking examples:
Example 1:
During one winter at the Arnhem Zoo, before releasing the chimps, the keepers hosed out all rubber tires in the enclosure and hung them on a horizontal log. One day, Krom was interested in a tire in which water had stayed behind. Unfortunately, this particular tire was at the end of the row, with six or more heavy tires in front of it. Krom
pulled and pulled at the one she wanted but couldn't remove it. She worked in vain for over ten minutes, ignored by everyone, except Jakie, a seven-year-old Krom had taken care of as a juvenile.
Immediately after Krom gave up and walked away, Jakie approached the scene. Without hesitation he pushed the tires one by one off the log, beginning with the front one, followed by the second, and so on, as any sensible chimp would. When he reached the last tire, he carefully removed it so that no water was lost, carrying it straight to his aunt, placing it upright in front of her. Krom accepted his present without any acknowledgment, and was already scooping up water with her hand when Jakie left (de Waal 1996, p. 83).
Example 2:
The two-meter-deep moat in front of the old bonobo enclosure at the San Diego Zoo had been drained for cleaning. After having scrubbed the moat and released the apes, the keepers went to turn on the valve to refill it with water when all of a sudden the old male, Kakowet, came to their window, screaming and frantically waving his arms so as to catch their attention. After so many years, he was familiar with the cleaning routine. As it turned out, several young bonobos had entered the dry moat but were unable to get out. The keepers provided a ladder. All bonobos got out except for the smallest one, who was pulled up by Kakowet himself (deWaal 1997a, p. 34).
Because it is almost impossible, and probably unethical, to create situations in the laboratory in which primates experience intense fear or distress, there is a scarcity of experiments on costly altruism of the kind described above. More often, experiments concern low-cost altruism, sometimes called "other-regarding preferences." A typical paradigm
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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. Colman et al. (1969) found 1 out of 4 tested macaques to be consistently other-regarding, yet two recent replications failed to find the same tendency in chimpanzees (Jensen et al. 2006, Silk et al. 2005). This has led authors to conclude that other-regarding preferences may be uniquely human. It is impossible to prove the null hypothesis, however. Given the overwhelming observational evidence for spontaneous helping and cooperation among primates, it seems only a matter of time until other-regarding preferences will be experimentally confirmed.
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, inner one. This is relevant to the origin of empathy: All prosocial behavior, even when dependent on prefrontal functioning, probably has PAM-based emotion sharing at its core (Preston & de Waal 2002 a). Without this emotional component, it is hard to see why we or other animals would care.
Humans have so little control over em-pathic activation that they regularly shield themselves from it, e.g., by covering their eyes when in a movie something gruesome is about to happen. This is because they have already identified with the on-screen characters. One way to cognitively control empathy is to inhibit such identification. How self-imposed filters and contextual appraisal modulate the brain's empathic response remains a major unresolved issue (de Vignemont & Singer 2006). Sometimes, empathy appears wholly absent. For example, chimpanzees are capable of brutally killing each other (de Waal 1998 [1982], Wrangham & Peterson 1996),
hence must be capable of suppressing empathic activation in relation to conspecifics, which has led Goodall (1986, p. 532) to call their victims "dechimpized." (It is important to note, though, that a species' occasional violence by no means argues against it having empathic capacities—if so, human empathy would be the first to be denied.)
The PAM model predicts that the greater the similarity or familiarity of the subject and object, the more their representations will agree, hence the more accurate their state-matching. Generally, the empathic response is amplified by similarity, familiarity, social closeness, and positive experience with the other (Table 1 in Preston & de Waal 2002a). In human studies, subjects empathize with a confederate's pleasure or distress if they perceive the relationship as cooperative, yet show an antipathic response (i.e., 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, Zillmann & Cantor 1977). These effects of previous experience have recently been confirmed by functional magnetic resonance imaging: Seeing the pain of a cooperative confederate activates pain-related brain areas, but seeing the pain of an unfair confederate activates reward-related brain areas, at least in men (Singer et al. 2006).
Relationship effects are also known for rodents, in which emotional contagion is measurable between cagemates but not between strangers (Langford et al. 2006). In monkeys, empathic responses to another's fear or pain are enhanced by familiarity between subject and object (Masserman et al. 1964, Miller at al. 1959). Thus, the empathy mechanism is biased the way evolutionary theory would predict. Empathy is (a) activated in relation to those with whom one has a close or positive relationship, and (b) suppressed, or even turned into Schadenfreude, in relation to strangers and defectors. The latter, retaliatory aspect corresponds with well-documented chimpanzee behavior: These apes not only
ivTinv.annualreviezvs.org • The Evolution of Empathy
reciprocate favors within positive relationships, but also take revenge upon those who have previously acted against them (de Waal & Luttrell 1988).
A common way in which mutually beneficial exchanges are achieved is through investment in long-term bonds to which both parties contribute. This reciprocity mechanism is commonplace in nonhuman primates (de Waal & Brosnan 2006) and has been suggested for human relations as well. Individual interests may be served by partnerships (e.g., marriages, friendships) that create a long-lasting communal "fitness interdependence" mediated by mutual empathy. Within these relationships, partners do not necessarily keep careful track of who did what for whom (Clark & Mills 1979), and derive psychological and health benefits not only from receiving but also from giving support (Brown & Brown 2006).
If altruism is produced by mechanisms, such as empathy and bonding, that produce emotional identification with the other, one may well ask if helping another does not boil down to helping oneself. It does, but as Smith (1759) argued, this is no reason to call empathy-based altruism selfish. A truly selfish individual would have no trouble walking away from another in need, whereas empathic engagement hooks one into the other's situation. Since the mechanism delivers intrinsic rewards exclusively via the other, it is genuinely other-oriented (Wispe 1991). At the same time, it is futile to try to extract the self from the process. There simply is no satisfactory answer to the question of how altruistic is altruism (debated among Batson et al. 1997, Cialdini et al. 1997, Hornstein 1991, Krebs 1991). This is, in fact, 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.
CONCLUSION
More than three decades ago, biologists deliberately removed the altruism from altruism. There is now increasing evidence that the brain is hardwired for social connection, and that the same empathy mechanism proposed to underlie human altruism (Batson 1991) may underlie the directed altruism of other animals. Empathy could well provide the main motivation making individuals who have exchanged benefits in the past to continue doing so in the future. Instead of assuming learned expectations or calculations about future benefits, this approach emphasizes a spontaneous altruistic impulse and a mediating role of the emotions. It is summarized in the five conclusions below:
1. An evolutionarily parsimonious account (cf. de Waal 1999) of directed altruism assumes similar motivational processes in humans and other animals.
2. Empathy, broadly defined, is a phyloge-netically ancient capacity.
3. Without the emotional engagement brought about by empathy, it is unclear what could motivate the extremely costly helping behavior occasionally observed in social animals.
4. Consistent with kin selection and reciprocal altruism theory, empathy favors familiar individuals and previous coop-erators, and is biased against previous defectors.
5. Combined with perspective-taking abilities, empathy's motivational autonomy opens the door to intentionally altruistic altruism in a few large-brained species.
ACKNOWLEDGMENTS
The author is grateful to Stephanie Preston for detailed comments on an earlier draft of the manuscript and to Jean Decety, Nancy Eisenberg, and Robert Trivers for constructive feedback. The author, however, remains responsible for the intellectual content.
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Contents
Annual Review of Psychology
Volume 59, 2008
Prefatory
The Evolution of a Cognitive Psychologist: A Journey from Simple
Behaviors to Complex Mental Acts
Gordon H. Bower............................................................................1
Pharmacology and Behavior
Addiction and the Brain Antireward System
George F. Koob and Michel he Moal......................................................29
Consummately Behavior
The Brain, Appetite, and Obesity
Hans-Rudolf Berthoud and Christopher Morrison.......................................55
Sex
Neuroendocrine Regulation of Feminine Sexual Behavior: Lessons from Rodent Models and Thoughts About Humans
Jeffrey D. Blaustein .......................................................................93
Audition and Its Biological Bases
The Biological Basis of Audition
Gregg H. Recanzone and Mitchell L. Sutter............................................119
Color Perception
Color in Complex Scenes
Steven K. Shevell and Frederick A.A. Kingdom........................................143
Scene Perception, Event Perception, or Object Recognition
Visual Perception and the Statistical Properties of Natural Scenes Wilson S. Geisler ........................................................
167
Cognitive Processes
The Mind and Brain of Short-Term Memory
John Jonides, Richard L. Lewis, Derek Evan Nee, Cindy A. Lustig, Marc G. Berman, and Katherine Sledge Moore ......................................193
Memory
Relativity of Remembering: Why the Laws of Memory Vanished
Henry L. Roediger, III....................................................................225
Reasoning and Problem Solving
Dual-Processing Accounts of Reasoning, Judgment, and Social Cognition
Jonathan St. B.T. Evans.................................................................255
Comparative Psychology, Ethology, and Evolution
Putting the Altruism Back into Altruism: The Evolution of Empathy
EransB.M. de Waal......................................................................279
Anxiety Disorders
Social Bonds and Posttraumatic Stress Disorder
Anthony Charuvastra andMarylene Cloitre ...........................................301
Inference, Person Perception, Attribution
Spontaneous Inferences, Implicit Impressions, and Implicit Theories
James S. Uleman, S. AdilSaribay, and Celia M. Gonzalez...........................329
Social Development, Social Personality, Social Motivation, Social Emotion
Motives of the Human Animal: Comprehending, Managing, and Sharing Inner States
E. Tory Higgins and Thane S. Pittman.................................................361
Cognition in Organizations
Cognition in Organizations
Gerard P. Hodgkinson and Mark P. Healey.............................................387
Selection and Placement
Personnel Selection
Paul R. Sackett and Filip Lievens .......................................................419
Contents
Education of Special Populations
The Education of Dyslexic Children from Childhood to Young Adulthood
Sally E. Shaywitz, Robin Morris, and Bennett A. Shaywitz...........................451
Health Promotion and Disease Prevention
Health Psychology: The Search for Pathways Between Behavior and Health
Howard Leventhal, John Weinman, Elaine A. Leventhal, and L. Alison Phillips____477
Emotion
Human Abilities: Emotional Intelligence
John D. Mayer, Richard D. Roberts, and Sigal G. Barsade............................507
Data Analysis
Sample Size Planning for Statistical Power and Accuracy in Parameter Estimation
Scott E. Maxwell, Ken Kelley, and Joseph R. Rausch ..................................537
Timely Topics
A Comprehensive Review of the Placebo Effect: Recent Advances and Current Thought
Donald D. Price, Damien G. Finniss, and Fabrizio Benedetti ........................565
Children's Social Competence in Cultural Context
Xinyin Chen and Dor an C. French .....................................................591
Grounded Cognition
Lawrence W. Barsalou ...................................................................617
Neuroeconomics
George Loewenstein, Scott Rick, and Jonathan D. Cohen .............................647
Indexes
Cumulative Index of Contributing Authors, Volumes 49-59 ........................673
Cumulative Index of Chapter Titles, Volumes 49-59 .................................678
Errata
An online log of corrections to Annual Review of Psychology articles may be found at http://psych.annualreviews.org/errata.shtml
Contents