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mise à jour du 16 mai 2002
Yearbook of physical anthropology
2001; 44; 3-24
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Human facial expressions as adaptations : evolutionary questions in facial expression research
Karen L. Schmidt and Jeffrey F. Cohn
Departments of Psychology and Anthropology, and Departments of Psychology and Psychiatry, University of Pittsburgh, Pittsburgh, Pennsylvania 15260
 Cortical Systems for the Recognition of Emotion in Facial Expressions
Yawning: an evolutionary perspective Smith EO
The perception-behavior expressway:automatic effects of social perception on social behavior
Response properties of neurons in temporal cortical visual areas of infant monkeys Rodman HR


Resume : The importance of the face in social interaction and social intelligence is widely recognized in anthropology. Yet the adaptive functions of human facial expression remain largely unknown. An evolutionary model of human facial expression as behavioral adaptation can be constructed, given the current knowledge of the phenotypic variation, ecological contexts, and fitness consequences of facial behavior. Studies of facial expression are available, but results are not typically framed in an evolutionary perspective. This review identifies the relevant physical phenomena of facial expression and integrates the study of this behavior with the anthropological study of communication and sociality in general. Anthropological issues with relevance to the evolutionary study of facial expression include: facial expressions as coordinated, stereotyped behavioral phenotypes, the unique contexts and functions of different facial expressions, the relationship of facial expression to speech, the value of facial expressions as signals, and the relationship of facial expression to social intelligence in humans and in nonhuman primates. Human smiling is used as an example of adaptation, and testable hypotheses concerning the human smile, as well as other expressions, are proposed.


Homology in facial expressions Game theoretic models of facial signaling assume the actors have the alternative of not signaling at all, and may refer to a past generation where signaling did not yet exist (Bradbury and Vehrencamp, 2000). Although these issues are theoretically important, the phylogeny of humans and the long prehistory of sociality in the Primate order make it somewhat unlikely that signaling with human facialexpression would disappear completely in humans. This is immediately apparent when considering the drastic and deeply damaging social consequences of facial paralysis (VanSwearingen et al., 1999). These and other forms of complete facial paralysis have such negative social consequences that it is difficult to imagine the lack of facial signaling as an alternative. In some cases, the amount of depression associated with facial paralysis is directly related to the degree of disability in producing a prototypical smile (VanSwearingen et al., 1999). It remains to be demonstrated, however, whether human facial expressions function adaptively, or whether they are simply remnants of a prelinguistic past (Darwin, 1872/ 1998). Clearly, though, there are differences in the frequency and intensity of facial expression across normal individuals. Facial expressions are not always produced when they would be advantageous, and this may lead to negative fitness consequences that are less dramatic than those discussed above, but still potentially costly in social interaction, depending on cultural and social context. Negative fitness consequences here are conceptualized as reduced access to cooperative relationships that tend to enhance survival and reproductive potential. Given the long history of sociality in our lineage and the ubiquity of facial expression in observations of naturalistic social interaction, we hypothesize that a certain level of facial expression must be obtained, or the individual risks losing the fitness benefits acquired during earlier interactions.

The homology of human and nonhuman primate facial expression may illustrate continuity among facial expression phenotypes, especially between apes and humans. Preuschoft and van Hooff (1995) note the remarkable stereotypy of facial expression across an order that is usually known for its behavioral flexibility. Production of basic facial expressions, such as the fear grimace in rhesus macaques,also appears to be highly canalized (Geen, 1992). It would be surprising if the level of stereotypy and homology in nonhuman primate expression did not extend to at least some patterns of human expression. Particular expressions, notably the silent bared teeth and relaxed open mouth displays, have been compared to the human smile and laughter (Chevalier-Skolnikoff, 1973; Darwin, 1872/1998; Preuschoft,1992; Preuschoft and van Hooff, 1995; van Hooff, 1972). Given the similar structure of the facial muscles and adaptations for focusing on the face, homologybetween nonhuman primate and human facial expressions has been suggested (van Hooff, 1972). The smile has been proposed as a homologue to the silent bared teeth display (SBT), and the laugh as homologue to relaxed open mouth displays of monkeys and apes (van Hooff, 1972; Preuschoft, 1992; Preschoft and van Hooff, 1995). Preuschoft (2000) suggests that the apparent contrast between the smile of humans (upward lip corners) and the SBT of nonhuman primates may simply be the result of similar muscles stretched over a very differentshapedmuzzle (Preuschoft, 2000).

In addition, there are common neurobiological bases among humans and other primates in the control of facial expression. A recent study of projections from the cortex to the facial nerve nucleus in rhesus macaques found a pattern similar to that described by Rinn (1984). Bilateral cortical projections to facial nuclei control frontalis and orbicularis oculi muscles, and contralateral projections to the opposite facial nucleus, control the muscles aroundthe mouth, allowing hemispheric differences in expressiveness to influence the lower face in particular (Morecraft et al., 2001). Researchers have begun to demonstrate asymmetry in facial expressions of monkeys, indicating that these underlying mechanisms of control also produce similar effects in non-human primates. Hook-Costigan and Rogers (1998) found that positive social calls and expressions of marmosets were lateralized to the right, while negative social expressions (fear) were lateralized to the left. Hauser and Akre (2001) also found that expressions were seen earlier on the left side of the face in rhesus macaques, although they found no different between expressions interpreted as socially positive or negative, expanding on the original finding by Hauser (1996) that rhesus expressions were leftsided. Although at least some degree of neurobiological and physical homology of expression seems likely, there is also the problem of differential function. Can human smiles really be homologous to the SBT display when human smiles signal joy and nonhuman primate smiles signal appeasement or fear? From the perspective of human facial expression, the roles of the smile continue to expand with new research, and the equation of human smiles withhappiness has been called into question (Ekman, 1985; Fridlund, 1994). Nonhuman primate bared teeth displays (as in Fig. 6) may be similar in meaning and function to human smiles, depending on the socioecological context. Human anger expressions and ape anger/fear expressions may also be homologous (Chevalier-Skolnikoff, 1973). Embarrassment has been proposed as a homologue of primate appeasement displays, because it shares characteristics such as withdrawal, minimizing appearance, and smile with downward glance (Keltner and Buswell, 1997). Homology has also been proposed for the yawn, which shows evidence of being a social signal of transition between activity states both in humans and in nonhuman primates (Deputte, 1994; Provine, 1997). Homology may also apply to aspects of hiding or minimizing expression. There are several examples of apes preventing conspecifics from seeing their expression by covering the face with a hand (Tomasello and Call, 1997), and one report of a chimp that was able to control a grimacing mouth by pressing down on his lips with his hand (Mitchell, 1999).Humans also move their hands to the face to hide expressions, possibly because such expressions would be detrimental to their interests if openly recognized (Keltner and Buswell, 1997) for embarrassment; see Provine (1997) for yawning.

Humans have the additional ability of hiding their expressions with the actions of other facial muscles, especially around the mouth where the downward pull of the depressor anguli oris muscle can somewhat conceal the rise of the lip corners due to the action of zygomaticus major (Ekman, 1985). Spontaneous expressions may have elements of concealment associated with them, such as "twisting" the smile to avoid appearing too pleased in front of others (Friedman and Miller-Herringer, 1991). In the same study, the authors noted that hand contact increased with increased smiling. It could be that the action of other facial muscles in some cases was inadequate to the task of concealing the increasingly obvious smile signal. Consideration of nonhuman primate facial expression, of course, is necessarily be specific to each individual species. Divergent facial signaling systems, as well as some homology, are to be expected. For the relationship between overall amount of expression and the structure of the facial nerve nucleus, Peburn et al. (2000) found variation betweenspecies, with the relatively more expressive macaques (Macaca fascicularis) showing significantly larger and better defined facial subnuclei than the relatively less expressive patas monkeys (Erythrocebus patas). Aotus, the only nocturnal anthropoid, has virtually no facial expression, and its facial musculature is also relatively less differentiated (Chevalier- Skolnikoff, 1973; Huber, 1931).

Likewise, many features of human facial expression, although universal, are specific to our species. The relative hairlessness of the human face, compared to the majority of nonhuman primates, suggests that the combination of exposed skin and retainedhair may have some signaling value. Brows are an important component of human greeting andsurprise displays, as well as some smiles. Upturned inner brows also signal sadness or grief (Eibl-Eibesfeldt, 1989; Ekman, 1979). Results of an intriguingstudy in which cross-species perception offacial expression was tested, the brows, a highlyvisible signal on the hairless human face, are notused by macaques seeking to identify sad humanfacial expressions. They rely instead on other, morephylogenetically conserved traits, such as cheekmovement (Kanazawa, 1998). Retention of facialhair in adult male humans may also play a role inaccentuating or concealing expression. Unfortunately,there has been no research on male facialhair as it relates to facial expression.Functions of facial expressions in nonhumanprimatesLike humans, many nonhuman primate speciespay close attention to the faces of other group members.

The complexity of face perception and facial expression among the great apes, for example, is just beginning to be demonstrated. Chimpanzees can use facial features to recognize both kin andunfamiliar conspecifics, and to categorize facial expressionsof other chimpanzees (Parr et al., 1998,2000; Parr and deWaal, 1999). Chimpanzees canfollow the gaze of another individual by paying attentionto its face (Povinelli and Eddy, 1996). Gorillas,chimpanzees, and bonobos have all been reportedto monitor the gaze of others, in ways thatsuggest they may be able to anticipate the impact oftheir facial expressions on others' behavior (Mitchell,1999). Clearly, facial expressions are importantsignals in the social lives of most nonhuman primates,just as they are for humans.By monitoring facial expressions, the intentions ofothers can be inferred. Because of their relativelystable existence, social groups provide an environmentin which low-cost, redundant signals can helpprimates to keep track of the other individual, possiblysimilar to that which Chadwick-Jones (1998)described for baboons. Cheater males may fail togive continuous signals, and so must be monitored.The failure to adhere to social scripts, includingfacial expression patterns, draws attention to uncooperative individuals (Mitchell, 1999). Groups of nonhuman primates may also utilize redundant,"cheap" vocal signals in order to coordinate theiractivities (Silk et al., 2000). Haslam (1997) provideda list of social grammars for primate interaction,including communal sharing, authority ranking,equality matching, and market pricing.These arebehavioral contexts of the type that could correspondto functional variation in primate facial expression.As in humans, considering facial expressionsas adaptations would require specification ofrelevant phenotypes, ecological contexts, and positiveand negative fitness consequences.

CONCLUSIONS : Current functional approaches to facial expression are largely framed in terms of the proximate functions of emotions associated with that expression(Keltner and Gross, 1999; Keltner and Haidt,1999; Yik and Russell, 1999). Fridlund (1994) hasargued from a critical psychological perspective forthe consideration of all facial behavior in a behavioralecological or evolutionary framework.

Evolutionary approaches, however, are necessarily basedon the study of facial expressions as biological adaptations,and much of the recent work on facial expression has been conducted outside this perspective. Nevertheless, results from this type offunctional study of facial expression provide a basison which to base evolutionary hypotheses of facial behavior. By detailing the phenotypic variation infacial expression, clearly defining the ecological contextsof facial expression, and describing some of thepositive fitness consequences of these behaviors, wehave outlined an evolutionary approach to the study of human facial expressions as adaptations. By proposing testable hypotheses about the nature of facial expression, we can also provide a firm biological basis to other anthropological studies of communication. The unfortunate, and probably unintended,view of nonverbal expression as representing an ancestral-primate primitive ability, whilelanguage is uniquely specialized in humans, canalso be challenged from this perspective (Eibl-Eibesfeldt, 1989). Instead of just assuming that nonverbal expression has much in common with primate relatives, but is also culturally patterned, w emay be in a position to specify more clearly theadaptive role of facial expression in human social interaction.Human social intelligence is obviously a major contributor to human brain evolution and intellectualabilities. Our most specialized and adaptive system of social signaling is human language (Pinker, 1994). Remarkable in its complexity andalso because of its seeming discontinuity with nonhuman primate vocalization and communication, human language has clear adaptive consequences for human evolution (Burling, 1993; Pinker, 1994).There is no doubt that language has been a driving force in the evolution of human behavior, and the social context is dominated by language (Dunbar,1996). Yet there is more to social intelligence than language. Deficits in other social skills, including nonverbal skills, make it very clear that language alone is not sufficient for successful social interaction,and the positive consequences of these skills are only now being described. This argues for increased attention to the evolution of nonverbal signaling systems, including facial expression, from theperspective of physical anthropology.