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Primates and Philosophers:
How Morality Evolved
Frans de Waal
Edited by Stephen Macedo & Josiah Ober

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Frans de Waal

We approve and we disapprove because we cannot do otherwise. Can we help feeling pain when the fire burns us? Can we help sympathizing with our friends?
   —Edward Westermarck (1912 [1908]: 19)
Why should our nastiness be the baggage of an apish past and our kindness uniquely human? Why should we not seek continuity with other animals for our “noble” traits as well?
   —Stephen Jay Gould (1980: 261)
Homo homini lupus —“man is wolf to man”—is an ancient Roman proverb popularized by Thomas Hobbes. Even though its basic tenet permeates large parts of law, economics, and political science, the proverb contains two major flaws. First, it fails to do justice to canids, which are among the most gregarious and cooperative animals on the planet (Schleidt and Shalter 2003). But even worse, the saying denies the inherently social nature of our own species.

Social contract theory, and Western civilization with it, seems saturated with the assumption that we are asocial, even nasty creatures rather than the zoon politikon that Aristotle saw in us. Hobbes explicitly rejected the Aristotelian view by proposing that our ancestors started out autonomous and combative, establishing community life only when the cost of strife became unbearable. According to Hobbes, social life never came naturally to us. He saw it as a step we took reluctantly and “by covenant only, which is artificial” (Hobbes 1991 [1651]: 120). More recently, Rawls (1972) proposed a milder version of the same view, adding that humanity’s move toward sociality hinged on conditions of fairness, that is, the prospect of mutually advantageous cooperation among equals.

These ideas about the origin of the well-ordered society remain popular even though the underlying assumption of a rational decision by inherently asocial creatures is untenable in light of what we know about the evolution of our species. Hobbes and Rawls create the illusion of human society as a voluntary arrangement with self-imposed rules assented to by free and equal agents. Yet, there never was a point at which we became social: descended from highly social ancestors—a long line of monkeys and apes—we have been group-living forever. Free and equal people never existed. Humans started out—if a starting point is discernible at all—as interdependent, bonded, and unequal. We come from a long lineage of hierarchical animals for which life in groups is not an option but a survival strategy. Any zoologist would classify our species as obligatorily gregarious.

Having companions offers immense advantages in locating food and avoiding predators (Wrangham 1980; van Schaik 1983). Inasmuch as group-oriented individuals leave more offspring than those less socially inclined (e.g., Silk et al. 2003), sociality has become ever more deeply ingrained in primate biology and psychology. If any decision to establish societies was made, therefore, credit should go to Mother Nature rather than to ourselves.

This is not to dismiss the heuristic value of Rawls’s “original position” as a way of getting us to reflect on what kind of society we would like to live in. His original position refers to a “purely hypothetical situation characterized so as to lead to certain conceptions of justice” (Rawls 1972: 12). But even if we do not take the original position literally, hence adopt it only for the sake of argument, it still distracts from the more pertinent argument that we ought to be pursuing, which is how we actually came to be what we are today. Which parts of human nature have led us down this path, and how have these parts been shaped by evolution? Addressing a real rather than hypothetical past, such questions are bound to bring us closer to the truth, which is that we are social to the core.

A good illustration of the thoroughly social nature of our species is that, second to the death penalty, solitary confinement is the most extreme punishment we can think of. It works this way only, of course, because we are not born as loners. Our bodies and minds are not designed for life in the absence of others. We become hopelessly depressed without social support: our health deteriorates. In one recent experiment, healthy volunteers deliberately exposed to cold and flu viruses got sick more easily if they had fewer friends and family around (Cohen et al. 1997). While the primacy of connectedness is naturally understood by women—perhaps because mammalian females with caring tendencies have outreproduced those without for 180 million years—it applies equally to men. In modern society, there is no more effective way for men to expand their age horizon than to get and stay married: it increases their chance of living past the age of sixty-five from 65 to 90 percent (Taylor 2002).

Our social makeup is so obvious that there would be no need to belabor this point were it not for its conspicuous absence from origin stories within the disciplines of law, economics, and political science. A tendency in the West to see emotions as soft and social attachments as messy has made theoreticians turn to cognition as the preferred guide of human behavior. We celebrate rationality. This is so despite the fact that psychological research suggests the primacy of affect: that is, that human behavior derives above all from fast, automated emotional judgments, and only secondarily from slower conscious processes (e.g., Zajonc 1980, 1984; Bargh and Chartrand 1999).

Unfortunately, the emphasis on individual autonomy and rationality and a corresponding neglect of emotions and attachment are not restricted to the humanities and social sciences. Within evolutionary biology, too, some have embraced the notion that we are a self-invented species. A parallel debate pitting reason against emotion has been raging regarding the origin of morality, a hallmark of human society. One school views morality as a cultural innovation achieved by our species alone. This school does not see moral tendencies as part and parcel of human nature. Our ancestors, it claims, became moral by choice. The second school, in contrast, views morality as a direct outgrowth of the social instincts that we share with other animals. In the latter view, morality is neither unique to us nor a conscious decision taken at a specific point in time: it is the product of social evolution.

The first standpoint assumes that deep down we are not truly moral. It views morality as a cultural overlay, a thin veneer hiding an otherwise selfish and brutish nature. Until recently, this was the dominant approach to morality within evolutionary biology as well as among science writers popularizing this field. I will use the term “Veneer Theory” to denote these ideas, tracing their origin to Thomas Henry Huxley (although they obviously go back much further in Western philosophy and religion, all the way to the concept of original sin). After treating these ideas, I review Charles Darwin’s quite different standpoint of an evolved morality, which was inspired by the Scottish Enlightenment. I further discuss the views of Mencius and Westermarck, which agree with those of Darwin.

Given these contrasting opinions about continuity versus discontinuity with other animals, I then build upon an earlier treatise (de Waal 1996) in paying special attention to the behavior of nonhuman primates in order to explain why I think the building blocks of morality are evolutionarily ancient.


In 1893, for a large audience in Oxford, England, Huxley publicly reconciled his dim view of the natural world with the kindness occasionally encountered in human society. Huxley realized that the laws of the physical world are unalterable. He felt, however, that their impact on human existence could be softened and modified if people kept nature under control. Thus, Huxley compared humanity with a gardener who has a hard time keeping weeds out of his garden. He saw human ethics as a victory over an unruly and nasty evolutionary process (Huxley 1989 [1894]).

This was an astounding position for two reasons. First, it deliberately curbed the explanatory power of evolution. Since many consider morality the essence of humanity, Huxley was in effect saying that what makes us human could not be handled by evolutionary theory. We can become moral only by opposing our own nature. This was an inexplicable retreat by someone who had gained a reputation as “Darwin’s Bulldog” owing to his fierce advocacy of evolution. Second, Huxley gave no hint whatsoever where humanity might have unearthed the will and strength to defeat the forces of its own nature. If we are indeed born competitors, who don’t care about the feelings of others, how did we decide to transform ourselves into model citizens? Can people for generations maintain behavior that is out of character, like a shoal of piranhas that decides to turn vegetarian? How deep does such a change go? Would not this make us wolves in sheep’s clothing: nice on the outside, nasty on the inside?

This was the only time Huxley broke with Darwin. As Huxley’s biographer, Adrian Desmond (1994: 599), put it: “Huxley was forcing his ethical Ark against the Darwinian current which had brought him so far.” Two decades earlier, in The Descent of Man, Darwin (1982 [1871]) had unequivocally included morality in human nature. The reason for Huxley’s departure has been sought in his suffering at the cruel hand of nature, which had taken the life of his beloved daughter, as well as his need to make the ruthlessness of the Darwinian cosmos palatable to the general public. He had depicted nature as so thoroughly “red in tooth and claw” that he could maintain this position only by dislodging human ethics, presenting it as a separate innovation (Desmond 1994). In short, Huxley had talked himself into a corner.

Huxley’s curious dualism, which pits morality against nature and humanity against other animals, was to receive a respectability boost from Sigmund Freud’s writings, which throve on contrasts between the conscious and subconscious, the ego and superego, Love and Death, and so on. As with Huxley’s gardener and garden, Freud was not just dividing the world into symmetrical halves: he saw struggle everywhere. He explained the incest taboo and other moral restrictions as the result of a violent break with the freewheeling sexual life of the primal horde, culminating in the collective slaughter of an overbearing father by his sons (Freud 1962 [1913]). He let civilization arise out of the renunciation of instinct, the gaining of control over the forces of nature, and the building of a cultural superego (Freud 1961 [1930]).

Humanity’s heroic combat against forces that try to drag him down remains a dominant theme within biology today, as illustrated by quotes from outspoken Huxleyans. Declaring ethics a radical break with biology, Williams wrote about the wretchedness of nature, culminating in his claim that human morality is a mere by-product of the evolutionary process: “I account for morality as an accidental capability produced, in its boundless stupidity, by a biological process that is normally opposed to the expression of such a capability” (Williams 1988: 438).

Having explained at length that our genes know what is best for us, programming every little wheel of the human survival machine, Dawkins waited until the very last sentence of The Selfish Gene to reassure us that, in fact, we are welcome to chuck all of those genes out the window: “We, alone on earth, can rebel against the tyranny of the selfish replicators” (Dawkins 1976: 215). The break with nature is obvious in this statement, as is the uniqueness of our species. More recently, Dawkins (1996) has declared us “nicer than is good for our selfish genes,” and explicitly endorsed Huxley: “What I am saying, along with many other people, among them T. H. Huxley, is that in our political and social life we are entitled to throw out Darwinism, to say we don’t want to live in a Darwinian world” (Roes, 1997: 3; also Dawkins 2003).

Darwin must be turning in his grave, because the implied “Darwinian world” is miles removed from what he himself envisioned (see below). What is lacking in these statements is any indication of how we can possibly negate our genes, which the same authors at other times have depicted as all-powerful. Like the views of Hobbes, Huxley, and Freud, the thinking is thoroughly dualistic: we are part nature, part culture, rather than a well-integrated whole. Human morality is presented as a thin crust underneath of which boil antisocial, amoral, and egoistic passions. This view of morality as a veneer was best summarized by Ghiselin’s famous quip: “Scratch an ‘altruist,’ and watch a ‘hypocrite’ bleed” (Ghiselin 1974: 247; figure 1).

Veneer Theory has since been popularized by countless science writers, such as Wright (1994), who went so far as to claim that virtue is absent from people’s hearts and souls, and that our species is potentially but not naturally moral. One might ask: “But what about the people who occasionally experience in themselves and others a degree of sympathy, goodness, and generosity?” Echoing Ghiselin, Wright replies that the “moral animal” is essentially a hypocrite:

[T]he pretense of selflessness is about as much part of human nature as is its frequent absence. We dress ourselves up in tony moral language, denying base motives and stressing our at least minimal consideration for the greater good; and we fiercely and self-righteously decry selfishness in others. (Wright 1994: 344)

To explain how we manage to live with ourselves despite this travesty, theorists have called upon self-deception. If people think they are at times unselfish, so the argument goes, they must be hiding their true motives from themselves (e.g., Badcock 1986). In the ultimate twist of irony, anyone who fails to believe that we are fooling ourselves, and feels that genuine kindness actually exists in the world, is considered a wishful thinker, hence accused of fooling him-or herself.

Some scientists have objected, however:

It is frequently said that people endorse such hypotheses [about human altruism] because they want the world to be a friendly and hospitable place. The defenders of egoism and individualism who advance this criticism thereby pay themselves a compliment; they pat themselves on the back for staring reality squarely in the face. Egoists and individualists are objective, they suggest, whereas proponents of altruism and group selection are trapped by a comforting illusion. (Sober and Wilson 1998: 8–9)

These back-and-forth arguments about how to reconcile everyday human kindness with evolutionary theory seem an unfortunate legacy of Huxley, who had a poor understanding of the theory that he so effectively defended against its detractors. In the words of Mayr (1997: 250): “Huxley, who believed in final causes, rejected natural selection and did not represent genuine Darwinian thought in any way. . . . It is unfortunate, considering how confused Huxley was, that his essay [on ethics] is often referred to even today as if it were authoritative.”

It should be pointed out, though, that in Huxley’s time there was already fierce opposition to his ideas (Desmond 1994), some of which came from Russian biologists, such as Petr Kropotkin. Given the harsh climate of Siberia, Russian scientists traditionally were far more impressed by the battle of animals against the elements than against each other, resulting in an emphasis on cooperation and solidarity that contrasted with Huxley’s dog-eat-dog perspective (Todes 1989). Kropotkin’s (1972 [1902]) Mutual Aid was an attack on Huxley, but written with great deference for Darwin.

Although Kropotkin never formulated his theory with the precision and evolutionary logic available to Trivers (1971) in his seminal paper on reciprocal altruism, both pondered the origins of a cooperative, and ultimately moral, society without invoking false pretense, Freudian denial schemes, or cultural indoctrination. In this they proved the true followers of Darwin.


Evolution favors animals that assist each other if by doing so they achieve long-term benefits of greater value than the benefits derived from going it alone and competing with others. Unlike cooperation resting on simultaneous benefits to all parties involved (known as mutualism), reciprocity involves exchanged acts that, while beneficial to the recipient, are costly to the performer (Dugatkin 1997). This cost, which is generated because there is a time lag between giving and receiving, is eliminated as soon as a favor of equal value is returned to the performer (for treatments of this issue since Trivers 1971, see Axelrod and Hamilton 1981; Roth-stein and Pierotti 1988; Taylor and McGuire 1988). It is in these theories that we find the germ of an evolutionary explanation of morality that escaped Huxley.

It is important to clarify that these theories do not conflict by any means with popular ideas about the role of selfishness in evolution. It is only recently that the concept of “selfishness” has been plucked from the English language, robbed of its vernacular meaning, and applied outside of the psychological domain. Even though the term is seen by some as synonymous with self-serving, English does have different terms for a reason. Selfishness implies the intention to serve oneself, hence knowledge of what one stands to gain from a particular behavior. A vine may be self-serving by overgrowing and suffocating a tree; but since plants lack intentions, they cannot be selfish except in a meaningless, metaphorical sense. Unfortunately, in complete violation of the term’s original meaning, it is precisely this empty sense of “selfish” that has come to dominate debates about human nature. If our genes are selfish, we must be selfish, too, is the argument one often hears, despite the fact that genes are mere molecules, and hence cannot be selfish (Midgley 1979).

It is fine to describe animals (and humans) as the product of evolutionary forces that promote self-interests so long as one realizes that this by no means precludes the evolution of altruistic and sympathetic tendencies. Darwin fully recognized this, explaining the evolution of these tendencies by group selection instead of the individual and kin selection favored by modern theoreticians (but see, e.g., Sober and Wilson 1998; Boehm 1999). Darwin firmly believed his theory capable of accommodating the origins of morality and did not see any conflict between the harshness of the evolutionary process and the gentleness of some of its products. Rather than presenting the human species as falling outside of the laws of biology, Darwin emphasized continuity with animals even in the moral domain:

Any animal whatever, endowed with well-marked social instincts, the parental and filial affections being here included, would inevitably acquire a moral sense or conscience, as soon as its intellectual powers had become as well developed, or nearly as well developed, as in man. (Darwin 1982 [1871]: 71–72)

It is important to dwell on the capacity for sympathy hinted at here and expressed more clearly by Darwin elsewhere (e.g., “Many animals certainly sympathize with each other’s distress or danger” [Darwin 1982 (1871): 77]), because it is in this domain that striking continuities exist between humans and other social animals. To be vicariously affected by the emotions of others must be very basic, because these reactions have been reported for a great variety of animals and are often immediate and uncontrollable. They probably first emerged with parental care, in which vulnerable individuals are fed and protected. In many animals they stretch beyond this domain, however, to relations among unrelated adults (section 4 below).

In his view of sympathy, Darwin was inspired by Adam Smith, the Scottish moral philosopher and father of economics. It says a great deal about the distinctions we need to make between self-serving behavior and selfish motives that Smith, best known for his emphasis on self-interest as the guiding principle of economics, also wrote about the universal human capacity of sympathy:

How selfish soever man may be supposed, there are evidently some principles in his nature, which interest him in the fortune of others, and render their happiness necessary to him, though he derives nothing from it, except the pleasure of seeing it. (Smith 1937 [1759]: 9)

The evolutionary origin of this inclination is no mystery. All species that rely on cooperation—from elephants to wolves and people—show group loyalty and helping tendencies. These tendencies evolved in the context of a close-knit social life in which they benefited relatives and companions able to repay the favor. The impulse to help was therefore never totally without survival value to the ones showing the impulse. But, as so often, the impulse became divorced from the consequences that shaped its evolution. This permitted its expression even when payoffs were unlikely, such as when strangers were beneficiaries. This brings animal altruism much closer to that of humans than usually thought, and explains the call for the temporary removal of ethics from the hands of philosophers (Wilson 1975: 562).

Personally, I remain unconvinced that we need group selection to explain the origin of these tendencies—we seem to get quite far with the theories of kin selection and reciprocal altruism. Moreover, there is so much intergroup migration (hence gene flow) in nonhuman primates that the conditions for group selection do not seem fulfilled. In all of the primates, the younger generation of one sex or another (males in many monkeys, females in chimpanzees and bonobos) tends to leave the group to join neighboring groups (Pusey and Packer 1987). This means that primate groups are far from genetically isolated, which makes group selection unlikely.

In discussing what constitutes morality, the actual behavior is less important than the underlying capacities. For example, instead of arguing that food-sharing is a building block of morality, it is rather the capacities thought to underlie food-sharing (e.g., high levels of tolerance, sensitivity to others’ needs, reciprocal exchange) that seem relevant. Ants, too, share food, but likely based on quite different urges than those that make chimpanzees or people share (de Waal 1989a). This distinction was understood by Darwin, who looked beyond the actual behavior at the underlying emotions, intentions, and capacities. In other words, whether animals are nice to each other is not the issue, nor does it matter much whether their behavior fits our moral preferences or not. The relevant question rather is whether they possess capacities for reciprocity and revenge, for the enforcement of social rules, for the settlement of disputes, and for sympathy and empathy (Flack and de Waal 2000).

This also means that calls to reject Darwinism in our daily lives so as to build a moral society are based on a profound misreading of Darwin. Since Darwin saw morality as an evolutionary product, he envisioned an eminently more livable world than the one proposed by Huxley and his followers, who believe in a culturally imposed, artificial morality that receives no helping hand from human nature. Huxley’s world is by far the colder, more terrifying place.


Edward Westermarck, a Swedish Finn who lived from 1862 until 1939, deserves a central position in any debate about the origin of morality, since he was the first scholar to promote an integrated view including both humans and animals and both culture and evolution. That his ideas were underappreciated during his lifetime is understandable, because they flew in the face of the Western dualistic tradition that pits body against mind and culture against instinct.

Westermarck’s books are a curious blend of dry theorizing, detailed anthropology, and secondhand animal stories. The author was eager to connect human and animal behavior, but his own work focused entirely on people. Since at the time little systematic research on animal behavior existed, he had to rely on anecdotes, such as the one of a vengeful camel that had been excessively beaten on multiple occasions by a fourteen-year-old camel driver for loitering or turning the wrong way. The camel passively took the punishment; but a few days later, finding itself unladen alone on the road with the same driver, “seized the unlucky boy’s head in its monstrous mouth, and lifting him up in the air flung him down again on the earth with the upper part of the skull completely torn off, and his brains scattered on the ground” (Westermarck 1912 [1908]: 38).

We should not discard such unverified reports out of hand: stories of delayed retaliation abound in the zoo world, especially about apes and elephants. We now have systematic data on how chimpanzees punish negative actions with other negative actions (called a “revenge system” by de Waal and Luttrell 1988), and how a macaque attacked by a dominant member of its troop will turn around to redirect aggression against a vulnerable younger relative of its attacker (Aureli et al. 1992). These reactions fall under Westermarck’s retributive emotions, but for him the term “retributive” went beyond its usual connotation of getting even. It also covered positive emotions, such as gratitude and the repayment of services. Depicting the retributive emotions as the cornerstone of morality, Westermarck weighed in on the question of its origin while anticipating modern discussions of evolutionary ethics.

Westermarck is part of a long tradition, going back to Aristotle and Thomas Aquinas, which firmly anchors morality in the natural inclinations and desires of our species (Arnhart 1998, 1999). Emotions occupy a central role; it is well known that, rather than being the antithesis of rationality, emotions aid human reasoning. People can reason and deliberate as much as they want, but, as neuroscientists have found, if there are no emotions attached to the various options in front of them, they will never reach a decision or conviction (Damasio 1994). This is critical for moral choice, because if anything morality involves strong convictions. These convictions don’t—or rather can’t—come about through a cool rationality: they require caring about others and powerful “gut feelings” about right and wrong.

Westermarck (1912 [1908], 1917 [1908]) discusses, one by one, a whole range of what philosophers before him, most notably David Hume (1985 [1739]), called the “moral sentiments.” He classified the retributive emotions into those derived from resentment and anger, which seek revenge and punishment, and those that are more positive and prosocial. Whereas in his time few animal examples of the moral emotions were known—hence his reliance on Moroccan camel stories—we know now that there are many parallels in primate behavior. He also discusses “forgiveness,” and how the turning of the other cheek is a universally appreciated gesture. Chimpanzees kiss and embrace after fights, and these so-called reconciliations serve to preserve peace within the community (de Waal and van Roosmalen 1979). A growing literature exists on conflict resolution in primates and other mammals (de Waal 1989b, 2000; Aureli and de Waal 2000; Aureli et al. 2002). Reconciliation may not be the same as forgiveness, but the two are obviously related.

Westermarck also sees protection of others against aggression as resulting from what he calls “sympathetic resentment,” thus implying that this behavior rests on identification and empathy with the other. Protection against aggression is common in monkeys and apes and in many other animals, who stick up for their kin and friends. The primate literature offers a well-investigated picture of coalitions and alliances, which some consider the hallmark of primate social life and the main reason that primates have evolved such complex, cognitively demanding societies (e.g., Byrne and Whiten 1988; Harcourt and de Waal 1992; de Waal 1998 [1982]).

Similarly, the retributive kindly emotions (“desire to give pleasure in return for pleasure”: Westermarck 1912 [1908]: 93) have an obvious parallel in what we now call reciprocal altruism, such as the tendency to repay in kind those from whom assistance has been received. Westermarck adds moral approval as a retributive kindly emotion, hence as a component of reciprocal altruism. These views antedate the discussions about “indirect reciprocity” in the modern literature on evolutionary ethics, which revolve around reputation building within the larger community (e.g., Alexander 1987). It is truly amazing to see how many issues brought up by contemporary authors are, couched in somewhat different terms, already present in the writings of this Swedish Finn of a century ago.

The most insightful part of Westermarck’s work is perhaps where he tries to come to grips with what defines a moral emotion as moral. Here he shows that there is more to such emotions than raw gut feeling, as he explains that they “differ from kindred non-moral emotions by their disinterestedness, apparent impartiality, and flavour of generality” (Westermarck 1917 [1908]: 738–39). Emotions such as gratitude and resentment directly concern one’s own interests—how one has been treated or how one wishes to be treated— hence they are too egocentric to be moral. Moral emotions ought to be disconnected from one’s immediate situation: they deal with good and bad at a more abstract, disinterested level. It is only when we make general judgments of how anyone ought to be treated that we can begin to speak of moral approval and disapproval. It is in this specific area, famously symbolized by Smith’s (1937 [1759]) “impartial spectator,” that humans seem to go radically further than other primates.

Sections 4 and 5 discuss continuity between the two main pillars of human morality and primate behavior. Empathy and reciprocity have been described as the chief “prerequisites” (de Waal 1996) or “building blocks” of morality (Flack and de Waal 2000)—they are by no means sufficient to produce morality as we know it, yet they are indispensable. No human moral society could be imagined without reciprocal exchange and an emotional interest in others. This offers a concrete starting point to investigate the continuity that Darwin envisioned. The debate about Veneer Theory is fundamental to this investigation since some evolutionary biologists have sharply deviated from the idea of continuity by presenting morality as a sham so convoluted that only one species—ours—is capable of it. This view has no basis in fact, and as such stands in the way of a full understanding of how we became moral (table 1). My intention here is to set the record straight by reviewing actual empirical data.


Evolution rarely throws out anything. Structures are transformed, modified, co-opted for other functions, or “tweaked” in another direction—descent with modification, as Darwin called it. Thus, the frontal fins of fish became the front limbs of land animals, which over time turned into hoofs, paws, wings, hands, and flippers. Occasionally, a structure loses all function and becomes superfluous, but this is a gradual process, often ending in rudimentary traits rather than disappearance. We find tiny vestiges of leg bones under the skin of whales and remnants of a pelvis in snakes.

This is why to the biologist, a Russian doll is such a satisfying plaything, especially if it has a historical dimension. I own a doll that shows Russian President Vladimir Putin on the outside, within whom we discover, in this order, Yeltsin, Gorbachev, Brezhnev, Kruschev, Stalin, and Lenin. Finding a little Lenin and Stalin within Putin will hardly surprise most political analysts. The same is true for biological traits: the old always remains present in the new.

This is relevant to the debate about the origin of empathy, since the psychologist tends to look at the world through different eyes than the biologist. Psychologists sometimes put our most advanced traits on a pedestal, ignoring or even denying simpler antecedents. They thus believe in saltatory change, at least in relation to our own species. This leads to unlikely origin stories, postulating discontinuities with respect to language, which is said to result from a unique “module” in the human brain (e.g., Pinker 1994), or with respect to human cognition, which is viewed as having cultural origins (e.g., Tomasello 1999). True, human capacities reach dizzying heights, such as when I understand that you understand that I understand, et cetera. But we are not born with such “reiterated empathy,” as phenomenologists call it. Both developmentally and evolutionarily, advanced forms of empathy are preceded by and grow out of more elementary ones. In fact, things may be exactly the other way around. Instead of language and culture appearing with a Big Bang in our species and then transforming the way we relate to each other, Greenspan and Shanker (2004) propose that it is from early emotional connections and “proto conversations” between mother and child (cf. Trevarthen 1993) that language and culture sprang. Instead of empathy being an endpoint, it may have been the starting point.

Biologists prefer bottom-up over top-down accounts, even though there is definitely room for the latter. Once higher order processes have come into existence, they modify processes at the base. The central nervous system is a good example of top-down processing, as in the control the prefrontal cortex exerts over memory. The prefrontal cortex is not the seat of memory, but can “order” memory retrieval (Tomita et al. 1999). In the same way, culture and language shape expressions of empathy. The distinction between “being the origin of ” and “shaping” is a fundamental one, though, and I will argue here that empathy is the original, pre-linguistic form of inter-individual linkage that only secondarily has come under the influence of language and culture.

Bottom-up accounts are the opposite of Big Bang theories. They assume continuity between past and present, child and adult, human and animal, even between humans and the most primitive mammals. We may assume that empathy first evolved in the context of parental care, which is obligatory in mammals (Eibl-Eibesfeldt 1974 [1971]; MacLean 1985). Signaling their state through smiling and crying, human infants urge their caregiver to pay attention and move into action (Bowlby 1958). The same applies to other primates. The survival value of these interactions is obvious. For example, a female chimpanzee lost a succession of infants despite intense positive interest because she was deaf and did not correct positional problems (such as sitting on the infant, or holding it upside-down) in response to its distress calls (de Waal 1998 [1982]).

For a human characteristic, such as empathy, that is so pervasive, develops so early in life (e.g., Hoffman 1975; Zahn-Waxler and Radke-Yarrow 1990), and shows such important neural and physiological correlates (e.g., Adolphs et al. 1994; Rimm-Kaufman & Kagan 1996; Decety and Chaminade 2003) as well as a genetic substrate (Plomin et al. 1993), it would be strange indeed if no evolutionary continuity existed with other mammals. The possibility of empathy and sympathy in other animals has been largely ignored, however. This is partly due to an excessive fear of anthropomorphism, which has stifled research into animal emotions (Panksepp 1998; de Waal 1999, appendix A), and partly to the one-sided portrayal by biologists of the natural world as a place of combat rather than social connectedness.

What Is Empathy?

Social animals need to coordinate action and movement, collectively respond to danger, communicate about food and water, and assist those in need. Responsiveness to the behavioral states of conspecifics ranges from a flock of birds taking off all at once because one among them is startled by a predator to a mother ape who returns to a whimpering youngster to help it from one tree to the next by draping her body as a bridge between the two. The first is a reflex-like transmission of fear that may not involve any understanding of what triggered the initial reaction, but that is undoubtedly adaptive. The bird that fails to take off at the same instant as the rest of the flock may be lunch. The selection pressure on paying attention to others must have been enormous. The mother-ape example is more discriminating, involving anxiety at hearing one’s offspring whimper, assessment of the reason for its distress, and an attempt to ameliorate the situation.

There exists ample evidence of one primate coming to another’s aid in a fight, putting an arm around a previous victim of attack, or other emotional responses to the distress of others (to be reviewed below). In fact, almost all communication among nonhuman primates is thought to be emotionally mediated. We are familiar with the prominent role of emotions in human facial expressions (Ekman 1982), but when it comes to monkeys and apes—which have a homologous array of expressions (van Hooff 1967)—emotions seem equally important.

When the emotional state of one individual induces a matching or closely related state in another, we speak of “emotional contagion” (Hatfield et al. 1993). Even if such contagion is undoubtedly a basic phenomenon, there is more to it than simply one individual being affected by the state of another: the two individuals often engage in direct interaction. Thus, a rejected youngster may throw a screaming tantrum at its mother’s feet, or a preferred associate may approach a food possessor to beg by means of sympathy-inducing facial expressions, vocalizations, and hand gestures. In other words, emotional and motivational states often manifest themselves in behavior specifically directed at a partner. The emotional effect on the other is not a by-product, therefore, but actively sought.

With increasing differentiation between self and other, and an increasing appreciation of the precise circumstances underlying the emotional states of others, emotional contagion develops into empathy. Empathy encompasses—and could not possibly have arisen without—emotional contagion, but it goes beyond it in that it places filters between the other’s and one’s own state. In humans, it is around the age of two that we begin to add these cognitive layers (Eisenberg and Strayer 1987).

Two mechanisms related to empathy are sympathy and personal distress,which in their social consequences are each other’s opposites. Sympathy is defined as “an affective response that consists of feelings of sorrow or concern for a distressed or needy other (rather than the same emotion as the other person). Sympathy is believed to involve an other-oriented, altruistic motivation” (Eisenberg 2000: 677). Personal distress, on the other hand, makes the affected party selfishly seek to alleviate its own distress, which is similar to what it has perceived in the object. Personal distress is therefore not concerned with the situation of the empathy-inducing other (Batson 1990). A striking primate example is given by de Waal (1996: 46): the screams of a severely punished or rejected infant rhesus monkey will often cause other infants to approach, embrace, mount, or even pile on top of the victim. Thus, the distress of one infant seems to spread to its peers, which then seek contact to soothe their own arousal. Inasmuch as personal distress lacks cognitive evaluation and behavioral complementarity, it does not reach beyond the level of emotional contagion.

That most modern textbooks on animal cognition (e.g., Shettleworth 1998) fail to index empathy or sympathy does not mean that these capacities are not an essential part of animal lives; it only means that they are being overlooked by a science traditionally focused on individual rather than inter-individual capacities. Tool use and numerical competence, for instance, are seen as hallmarks of intelligence, whereas appropriately dealing with others is not. It is obvious, however, that survival often depends on how animals fare within their group, both in a cooperative sense (e.g., concerted action, information transfer) and in a competitive sense (e.g., dominance strategies, deception). It is in the socialdomain, therefore, that one expects the highest cognitive achievements. Selection must have favored mechanisms to evaluate the emotional states of others and quickly respond to them. Empathy is precisely such a mechanism.

In human behavior, there exists a tight relation between empathy and sympathy, and their expression in psychological altruism (e.g., Hornblow 1980; Hoffman 1982; Batson et al. 1987; Eisenberg and Strayer 1987; Wispé 1991). It is reasonable to assume that the altruistic and caring responses of other animals, especially mammals, rest on similar mechanisms. When Zahn-Waxler visited homes to find out how children respond to family members instructed to feign sadness (sobbing), pain (crying), or distress (choking), she discovered that children a little over one year of age already comfort others. Since expressions of sympathy emerge at an early age in virtually every member of our species, they are as natural as the first step. An unplanned sidebar to this study, however, was that household pets appeared as worried as the children by the “distress” of family members. They hovered over them or put their heads in their laps (Zahn-Waxler et al. 1984).

Rooted in attachment and what Harlow termed the “affectional system” (Harlow and Harlow 1965), responses to the emotions of others are commonplace in social animals. Thus, behavioral and physiological data suggest emotional contagion in a variety of species (reviewed in Preston and de Waal 2002b, and de Waal 2003). An interesting literature that appeared in the 1950s and ’60s by experimental psychologists placed the words “empathy” and “sympathy” between quotation marks. In those days, talk of animal emotions was taboo. In a paper provocatively entitled “Emotional Reactions of Rats to the Pain of Others,” Church (1959) established that rats that had learned to press a lever to obtain food would stop doing so if their response was paired with the delivery of an electric shock to a visible neighboring rat. Even though this inhibition habituated rapidly, it suggested something aversive about the pain reactions of others. Perhaps such reactions arouse negative emotions in rats that witness them.

Monkeys show a stronger inhibition than rats. The most compelling evidence for the strength of empathy in monkeys came from Wechkin et al. (1964) and Masserman et al. (1964). They found that rhesus monkeys refuse to pull a chain that delivers food to themselves if doing so shocks a companion. One monkey stopped pulling for five days, and another one for twelve days after witnessing shock delivery to a companion. These monkeys were literally starving themselves to avoid inflicting pain upon another. Such sacrifice relates to the tight social system and emotional linkage among these macaques, as supported by the finding that the inhibition to hurt another was more pronounced between familiar than unfamiliar individuals (Masserman et al. 1964).

Although these early studies suggest that, by behaving in certain ways, animals try to alleviate or prevent distress in others, it remains unclear if spontaneous responses to distressed conspecifics are explained by (a) aversion to distress signals of others, (b) personal distress generated through emotional contagion, or (c) true helping motivations. Work on nonhuman primates has furnished further information. Some of this evidence is qualitative, but quantitative data on empathic reactions exists as well.

Anecdotes of “Changing Places in Fancy”

Striking depictions of primate empathy and altruism can be found in Yerkes (1925), Ladygina-Kohts (2002 [1935]), Goodall (1990), and de Waal (1998 [1982], 1996, 1997a). Primate empathy is such a rich area that O’Connell (1995) was able to conduct a content analysis of thousands of qualitative reports. She concluded that responses to the distress of another seem considerably more complex in apes than monkeys. To give just one example of the strength of the ape’s empathic response, Ladygina-Kohts wrote about her young chimpanzee, Joni, that the best way to get him off the roof of her house (much better than any reward or threat of punishment) was by arousing his sympathy:

If I pretend to be crying, close my eyes and weep, Joni immediately stops his plays or any other activities, quickly runs over to me, all excited and shagged, from the most remote places in the house, such as the roof or the ceiling of his cage, from where I could not drive him down despite my persistent calls and entreaties. He hastily runs around me, as if looking for the offender; looking at my face, he tenderly takes my chin in his palm, lightly touches my face with his finger, as though trying to understand what is happening, and turns around, clenching his toes into firm fists. (Ladygina-Kohts, 2002 [1935]: 121)

De Waal (1996, 1997a) has suggested that apart from emotional connectedness, apes have an appreciation of the other’s situation and a degree of perspective-taking (appendix B). So, the main difference between monkeys and apes is not in empathy per se,but in the cognitive overlays, which allow apes to adopt the other’s viewpoint. One striking report in this regard concerns a bonobo female empathizing with a bird at Twycross Zoo, in England:

One day, Kuni captured a starling. Out of fear that she might molest the stunned bird, which appeared undamaged, the keeper urged the ape to let it go. . . . Kuni picked up the starling with one hand and climbed to the highest point of the highest tree where she wrapped her legs around the trunk so that she had both hands free to hold the bird. She then carefully unfolded its wings and spread them wide open, one wing in each hand, before throwing the bird as hard she could towards the barrier of the enclosure. Unfortunately, it fell short and landed onto the bank of the moat where Kuni guarded it for a long time against a curious juvenile. (de Waal, 1997a, p. 156)

What Kuni did would obviously have been inappropriate towards a member of her own species. Having seen birds in flight many times, she seemed to have a notion of what would be good for a bird, thus offering us an anthropoid version of the empathic capacity so enduringly described by Adam Smith (1937 [1759]: 10) as “changing places in fancy with the sufferer.” Perhaps the most striking example of this capacity is a chimpanzee who, as in the original Theory of Mind (ToM) experiments of Premack and Woodruff (1978), seemed to understand the intentions of another and provided specific assistance:

During one winter at the Arnhem Zoo, after cleaning the hall and before releasing the chimps, the keepers hosed out all rubber tires in the enclosure and hung them one by one on a horizontal log extending from the climbing frame. 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 hanging in front of it. Krom pulled and pulled at the one she wanted but couldn’t remove it from the log. She pushed the tire backward, but there it hit the climbing frame and couldn’t be removed either. Krom worked in vain on this problem 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 in the row, 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 special acknowledgment, and was already scooping up water with her hand when Jakie left. (Adapted from de Waal 1996)

That Jakie assisted his aunt is not so unusual. What is special is that he correctly guessed what Krom was after. He grasped his auntie’s goals. Such so-called “targeted helping” is typical of apes, but rare or absent in most other animals. It is defined as altruistic behavior tailored to the specific needs of the other even in novel situations, such as the highly publicized case of Binti Jua, a female gorilla who rescued a human child at the Brookfield Zoo in Chicago (de Waal, 1996, 1999). A recent experiment demonstrated targeted helping in young chimpanzees (Warneken and Tomasello 2006).

It is important to stress the incredible strength of the ape’s helping response, which makes these animals take great risks on behalf of others. Whereas in a recent debate about the origins of morality, Kagan (2000) considered it obvious that a chimpanzee would never jump into a cold lake to save another, it may help to quote Goodall (1990: 213) on this issue:

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.

The only other animals with a similar array of helping responses are dolphins and elephants. This evidence, too, is largely descriptive (dolphins: Caldwell and Caldwell 1966; Connor and Norris 1982; elephants: Moss 1988; Payne 1998), yet here again it is hard to accept as coincidental that scientists who have watched these animals for any length of time have numerous such stories, whereas scientists who have watched other animals have few, if any.

Consolation Behavior

This difference between monkey and ape empathy has been confirmed by systematic studies of a behavior known as “consolation,” first documented by de Waal and van Roosmalen (1979). Consolation is defined as reassurance by an uninvolved bystander to one of the combatants in a preceding aggressive incident. For example, a third party goes over to the loser of a fight and gently puts an arm around his or her shoulders (figure 2). Consolation is not to be confused with reconciliation between former opponents, which seems mostly motivated by self-interest, such as the imperative to restore a disturbed social relationship (de Waal 2000). The advantage of consolation for the actor remains wholly unclear. The actor could probably walk away from the scene without any negative consequences.

Information on chimpanzee consolation is well quantified. De Waal and van Roosmalen (1979) based their conclusions on an analysis of hundreds of postconflict observations, and a replication by de Waal and Aureli (1996) included an even larger sample in which the authors sought to test two relatively simple predictions. If third-party contacts indeed serve to alleviate the distress of conflict participants, these contacts should be directed more at recipients of aggression than at aggressors, and more at recipients of intense rather than mild aggression. Comparing third-party contact rates with baseline levels, the investigators found support for both predictions (figure 3).

Consolation has thus far been demonstrated in great apes only. When de Waal and Aureli (1996) set out to apply exactly the same observation methodology as used on chimpanzees to detect consolation in macaques, they failed to find any (reviewed by Watts et al. 2000). This came as a surprise, because reconciliation studies, which employ essentially the same data collection method, have shown reconciliation in species after species. Why, then, would consolation be restricted to apes?

Possibly, one cannot achieve cognitive empathy without a high degree of self-awareness. Targeted help in response to specific, sometimes novel, situations may require a distinction between self and other that allows the other’s situation to be divorced from one’s own while maintaining the emotional link that motivates behavior. In other words, in order to understand that the source of vicarious arousal is not oneself but the other and to understand the causes of the other’s state, one needs a clear distinction between self and other. Based on these assumptions, Gallup (1982) was the first to speculate about a connection between cognitive empathy and mirror self-recognition (MSR). This view is supported both developmentally, by a correlation between the emergence of MSR in young children and their helping tendencies (Bischof-Köhler 1988; Zahn-Waxler et al. 1992), and phylogenetically, by the presence of complex helping and consolation in hominoids (i.e., humans and apes) but not monkeys. Hominoids are also the only primates with MSR.

I have argued before that, apart from consolation behavior, targeted helping reflects cognitive empathy. Targeted helping is defined as altruistic behavior tailored to the specific needs of the other in novel situations, such as the previously described reaction of Kuni to the bird or Binti Jua’s rescue of a boy. These responses require an understanding of the specific predicament of the individual needing help. Given the evidence for targeted helping by dolphins (see above), the recent discovery of MSR in these mammals (Reiss and Marino 2001) supports the proposed connection between increased self-awareness, on the one hand, and cognitive empathy, on the other.

Russian Doll Model

The literature includes accounts of empathy as a cognitive affair, even to the point that apes, let alone other animals, probably lack it (Povinelli 1998; Hauser 2000). This view equates empathy with mental state attribution and ToM. The opposite position has recently been defended in relation to autistic children, however. Contra earlier assumptions that autism reflects a ToM deficit (Baron-Cohen 2000), autism is noticeable well before the age of 4 years at which ToM typically emerges. Williams et al. (2001) argue that the main deficit of autism concerns the socio-affective level, which in turn negatively impacts sophisticated downstream forms of interpersonal perception, such as ToM. Thus, ToM is seen as a derived trait, and the authors urge more attention to its antecedents (a position now also embraced by Baron-Cohen 2003, 2004).

Preston and de Waal (2002a) propose that at the core of the empathic capacity is a relatively simple mechanism that provides an observer (the “subject”) with access to the emotional 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 activated. The closer and more similar subject and object are, the easier it will be for the subject’s perception to activate motor and autonomic responses that match the object’s (e.g., changes in heart rate, skin conductance, facial expression, body posture). This activation allows the subject to get “under the skin” of the object, sharing its feelings and needs, which embodiment in turn fosters sympathy, compassion, and helping. Preston and de Waal’s (2002a) Perception-Action Mechanism (PAM) fits Damasio’s (1994) somatic marker hypothesis of emotions as well as recent evidence for a link at the cellular level between perception and action (e.g., “mirror neurons,” di Pelligrino et al. 1992).

The idea that perception and action share representations is anything but new: it goes as far back as the first treatise on Einfühlung, the German concept translated into English as “empathy” (Wispé 1991). When Lipps (1903) spoke of Einfühlung,which literally means “feeling into,” he speculated about innere Nachahmung (inner mimicry) of another’s feelings along the same lines as proposed by the PAM. Accordingly, empathy is a routine involuntary process, as demonstrated by electromyographic studies of invisible muscle contractions in people’s faces in response to pictures of human facial expressions. These reactions are fully automated and occur even when people are unaware of what they saw (Dimberg et al. 2000). Accounts of empathy as a higher cognitive process neglect these gut-level reactions, which are far too rapid to be under conscious control.

Perception-action mechanisms are well known for motor perception (Prinz and Hommel 2002), causing researchers to assume similar processes to underlie emotion perception (Gallese 2001; Wolpert et al. 2001). Data suggest that both observing and experiencing emotions involves shared physiological substrates: seeing another’s disgust or pain is very much like being disgusted or in pain (Adolphs et al. 1997, 2000; Wicker et al. 2003). Also, affective communication creates similar physiological states in subject and object (Dimberg 1982, 1990; Levenson and Reuf 1992). In short, human physiological and neural activity does not take place on an island, but is intimately connected with and affected by fellow human beings. Recent investigations of the neural basis of empathy lend strong support to the PAM (Carr et al. 2003; Singer et al. 2004; de Gelder et al. 2004).

How simple forms of empathy relate to more complex ones has been depicted as a Russian doll by de Waal (2003). Accordingly, empathy covers all forms of one individual’s emotional state affecting another’s, with basic mechanisms at its core and more advanced mechanisms and cognitive abilities as its outer layers (figure 4). Autism may be reflected in deficient outer layers of the Russian doll, but such deficiencies invariably go back to deficient inner layers.

This is not to say that higher cognitive levels of empathy are irrelevant, but they are built on top of this firm, hardwired basis without which we would be at a loss about what moves others. Surely, not all empathy is reducible to emotional contagion, but it never gets around it. At the core of the Russian doll, we find a PAM-induced emotional state that corresponds with the object’s state. In a second layer, cognitive empathy implies appraisal of another’s predicament or situation (cf. de Waal 1996). The subject not only responds to the signals emitted by the object, but seeks to understand the reasons for these signals, looking for clues in the other’s behavior and situation. Cognitive empathy makes it possible to furnish targeted help that takes the specific needs of the other into account (figure 5). These responses go well beyond emotional contagion, yet they would be hard to explain without the motivation provided by the emotional component. Without it, we would be as disconnected as Mr. Spock in Star Trek,constantly wondering why others feel what they say they feel.

Whereas monkeys (and many other social mammals) clearly seem to possess emotional contagion and a limited degree of targeted helping, the latter phenomenon is not nearly as robust as in the great apes. For example, at Jigokudani Monkey Park, in Japan, first-time mother macaques are kept out of the hot springs by park wardens because of the experience that these females will accidentally drown their infants. They fail to pay attention to them when submerging themselves in the ponds. This is something monkey mothers apparently have to learn with time, showing that they do not automatically take their offspring’s perspective. De Waal (1996) ascribed their behavioral change to “learned adjustment,” setting it apart from cognitive empathy, which is more typical of apes and humans. Ape mothers respond immediately and appropriately to the specific needs of their offspring. They are, for example, very careful to keep them away from water, rushing over to pull them away as soon as they get too close.

In conclusion, empathy is not an all-or-nothing phenomenon: it covers a wide range of emotional linkage patterns, from the very simple and automatic to the highly sophisticated. It seems logical to first try to understand the basic forms of empathy, which are widespread indeed, before addressing the variations that cognitive evolution has constructed on top of this foundation.

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File created: 8/7/2007

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