Human Facial Expressions as Adaptations:
Evolutionary Questions in Facial Expression Research
KAREN L. SCHMIDT
AND JEFFREY F. COHN
Departments of Psychology and Anthropology, University of Pittsburgh, Pittsburgh, Pennsylvania 15260
Departments of Psychology and Psychiatry, University of Pittsburgh, Pittsburgh, Pennsylvania 15260
KEY WORDS nonverbal communication; social intelligence; signaling systems
ABSTRACT The importance of the face in social inter-
action and social intelligence is widely recognized in an-
thropology. Yet the adaptive functions of human facial
expression remain largely unknown. An evolutionary
model of human facial expression as behavioral adapta-
tion can be constructed, given the current knowledge of
the phenotypic variation, ecological contexts, and ﬁtness
consequences of facial behavior. Studies of facial expres-
sion are available, but results are not typically framed in
an evolutionary perspective. This review identiﬁes the
relevant physical phenomena of facial expression and in-
tegrates the study of this behavior with the anthropolog-
ical study of communication and sociality in general. An-
thropological 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 expres-
sion to social intelligence in humans and in nonhuman pri-
mates. Human smiling is used as an example of adaptation,
and testable hypotheses concerning the human smile, as
well as other expressions, are proposed. Yrbk Phys An-
thropol 44:3–24, 2001. ©2001 Wiley-Liss, Inc.
TABLE OF CONTENTS
Introduction ................................................................................................................................................................. 4
Facial expressions as adaptations .......................................................................................................................... 4
Behavioral Phenotype Sets ......................................................................................................................................... 4
Anatomical variation and facial expression .......................................................................................................... 5
Variation in neural control of facial muscles ........................................................................................................ 6
Variation within facial expression phenotype sets ............................................................................................... 7
Individual differences in observable facial behavior ............................................................................................ 8
Methods in facial expression research ................................................................................................................... 9
Phenotypic variation in facial perception .............................................................................................................. 9
Diversity among facial expression phenotypes ................................................................................................... 10
Ecological Contexts and Fitness Consequences ..................................................................................................... 11
Facial expressions as social signals ..................................................................................................................... 11
Socioecological contexts of human facial expression .......................................................................................... 11
Infant/caregiver interaction .................................................................................................................................. 12
Long-term cooperative social interaction ............................................................................................................. 13
Positive ﬁtness consequences ............................................................................................................................... 15
Facial expressions during speech ......................................................................................................................... 15
Courtship and facial expression ........................................................................................................................... 16
Strangers, competitors, and conﬂicts of interest ................................................................................................. 16
Signal properties of facial displays ...................................................................................................................... 17
The functions of facial expression ........................................................................................................................ 18
Phylogenetic Perspectives on Facial Expression .................................................................................................... 18
Homology in facial expressions ............................................................................................................................ 18
Functions of facial expressions in nonhuman primates ..................................................................................... 20
Conclusions ................................................................................................................................................................ 20
Acknowledgments ...................................................................................................................................................... 20
Literature Cited ........................................................................................................................................................ 21
YEARBOOK OF PHYSICAL ANTHROPOLOGY 44:3–24 (2001)
©2001 WILEY-LISS, INC.
Facial expressions as adaptations
One of the central questions in human evolution is
the origin of human sociality and ultimately, human
culture. In the search for the origin of social intelli-
gence in humans, much attention is focused on the
evolution of the brain and consciousness. Many as-
pects of human cognition and behavior are best ex-
plained with reference to millions of years of evolu-
tion in a social context (Byrne, 1995; Cosmides et al.,
1992; Humphrey, 1976). Human brainpower can
thus be explained, in part, by increasing social de-
mands over the course of human prehistory (Dun-
bar, 1998). Social intelligence, however, is not re-
ﬂected only in the brain, but in every adaptation
that allows successful interaction in social groups.
New advances in studying the biology of social be-
havior have not fully explored that most visibly so-
cial part of the human body, the face. The face is a
visible signal of others’social intentions and moti-
vations, and facial expression continues to be a crit-
ical variable in social interaction.
Although social intelligence is an increasingly rich
source of hypotheses of cognitive and behavioral ad-
aptations, the anthropological study of facial expres-
sion remains focused on essentially nonadaptive
questions. Current anthropological views of facial
expression tend to focus on the contrasts between
universal and culture-speciﬁc explanations of facial
expressions. Facial expression is either interpreted
as a human universal, with basic expressions repre-
sented in all known human populations (Brown,
1990), or it is conceptualized as the natural out-
growth of cultural differences, with little overlap in
expression from population to population (Bird-
whistell, 1975). Physical anthropologists, with im-
portant exceptions (Blurton Jones, 1972; Fessler,
1999; and see Chevalier-Skolnikoff, 1973; Goodall,
1986; Hauser, 1996; Preuschoft and van Hooff, 1995
for comparison with nonhuman primates), have gen-
erally avoided the study of human facial expressions
and nonverbal communication, leaving the interpre-
tation of facial expression largely to psychology and
to other branches of anthropology (Birdwhistell,
1970; LaBarre, 1947). The current state of research
in facial expression, combined with the current in-
terest in social intelligence as a driving force in
human evolution, calls for the re-emergence of the
study of facial adaptation in physical anthropology.
Establishing human facial expressions as biologi-
cal adaptations requires a rigorous review of our
current knowledge and ultimately the formation and
testing of evolutionarily based hypotheses. The def-
inition by Reeve and Sherman (1993) of adaptation
is a guideline for developing evolutionary hypothe-
ses, and allows the exploration of behavioral adap-
tations that have remained relatively unknown in
physical anthropology. They deﬁne an adaptation as
“a phenotypic variant that results in the highest
ﬁtness among a speciﬁed set of variants in a given
environment.”This deﬁnition is particularly suited
to adaptive hypotheses of human behavior, because
its requirements can be met with observation of
current phenomena, and reference to phylogenetic
factors is not required (Reeve and Sherman, 1993).
What is required, however, is evidence of phenotypic
variation, well-deﬁned ecological contexts, and ﬁt-
ness consequences for a particular adaptation.
The purpose of this review is to provide a frame-
work for asking evolutionary, adaptive questions
about human facial expression. First, we establish
human facial expression as a potential behavioral
adaptation, by detailing the phenotypic variation,
ecological contexts, and ﬁtness consequences of fa-
cial behavior. A particular expression, the human
smile, is used as an example of the potential of the
adaptationist approach for understanding human
facial expression in an evolutionary perspective. Fi-
nally, facial behavior is compared to that of nonhu-
man primates to provide some further phylogenetic
perspective on the evolution of facial expression and
its role in the evolution of human social intelligence.
BEHAVIORAL PHENOTYPE SETS
Human universal facial expressions
are perhaps the most familiar examples of facial
expression, at least among anthropologists. Six ba-
sic expression categories have been shown to be
recognizable across cultures (see Fig. 1), and this
Notwithstanding Fridlund’s compelling arguments concerning the
use of the alternate term “facial display,”to describe facial actions,
this review will rely on the older term, “facial expression”for the sake
of simplicity. No emotional input is necessarily implied by the use of
the word expression.
Fig. 1. Basic facial expression phenotypes. 1, disgust; 2, fear;
3, joy; 4, surprise; 5, sadness; 6, anger. Posed images from Kanade
et al. (2000).
4YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 44, 2001
ﬁnding is generally accepted by psychologists work-
ing on facial expression. The six basic emotional
or facial conﬁgurations associated
with particular emotional situations, have been
shown to be universal in their performance and in
their perception (Ekman and Keltner, 1997), al-
though there is some objection to the idea that these
expressions signal similar emotions in people of dif-
ferent cultures (Fridlund, 1994; Russell and Fernan-
dez-Dols, 1997). The controversy surrounding the
attribution of universal emotions to universal facial
expressions of emotion is important for understand-
ing emotions cross-culturally. Nevertheless, even
those who disagree on the emotion concede the
cross-cultural consistency of the combinations of fa-
cial movements (behavioral phenotypes) that make
up expressions of “disgust,”“fear,”“joy,”“surprise,”
“sadness,”and “anger”(Russell and Fernandez-
Dols, 1997). These expressions were ﬁrst discussed
by Darwin (1872/1998) as universals, and have been
recognized in people from widely divergent cultural
and social backgrounds, as well as in the faces of
individuals born deaf and blind (Darwin, 1872/1998;
Eibl-Eibesfeldt, 1989; Izard, 1977; Ekman and Kelt-
In addition to the six basic facial expressions,
there are also coordinated, stereotyped nonverbal
displays that include stereotyped facial expression
components. These include the eyebrow ﬂash, yawn-
ing, startle, the coy display, and embarrassment and
shame displays (Eibl-Eibesfeldt, 1989; Grammer et
al., 1988; Keltner and Buswell, 1997; Keltner and
Harker, 1998; Provine, 1997). These displays typi-
cally combine both facial and postural or gestural
elements and are found in widely distributed popu-
lations, suggesting species rather than cultural
The eyebrow ﬂash is a good example of this kind of
display. The frontalis muscle is consistently used to
raise both medial and lateral parts of the eyebrow
(Ekman and Friesen, 1978; Grammer et al., 1988). A
common repertoire of synchronous facial movements
occurs in combination with the eyebrow ﬂash, in-
cluding most frequently the raising of the lip corners
(smile), and lifting of the upper lid (Grammer et al.,
1988). In addition to consistency in muscle action,
the timing of the eyebrow ﬂash is also consistent
cross-culturally in the three non-Western popula-
tions analyzed. The onset of the eyebrow ﬂash typi-
cally follows a pause in all other facial movements,
and takes about 100 msec, with very little variation
across cultural groups. In addition, coordinated
head movements are found in association with eye-
brow ﬂashes, extending the display beyond the face
itself (Grammer et al., 1988; and see Fig. 2).
In order to produce the eyebrow ﬂash and other
recognizable, universal expressions, humans pre-
sumably use the same facial musculature, and move
it into a similar conﬁguration under similar circum-
stances. Thus each of these coordinated facial dis-
plays can be considered a behavioral phenotype.
Within these facial expression phenotypes, however,
and across individual humans, there is a great deal
of physical variation in structure, movement, and
perception. Universal displays, together with varia-
tion around the basic components of these displays,
comprise what can be considered phenotype sets of
facial expression. Sources of this variation include
anatomical and neurobiological differences, as well
as demographic differences such as sex, age, and
cultural background. In addition, the perception of
facial expression, important for understanding com-
municative adaptations, is also a source of individ-
Anatomical variation and facial expression
The structure of human facial muscles has been
known for some time (Duchenne, 1859/1990; Huber,
1931; and see Fig. 3). The anatomical basis of facial
expression has been described in detail, and an an-
atomically based coding system is available for the
objective study of facial action (Facial Action Coding
System; Ekman and Friesen, 1978). This system
outlines speciﬁc actions produced by particular fa-
cial muscles. The quality of these actions, however,
likely varies with differences in the facial muscles.
Different facial muscles produce different types of
movements, and they are most likely heterogeneous
in their structure and innervation. Goodmurphy and
Ovalle (1999), for example, have shown that muscle
ﬁber types, shapes, and sizes in orbicularis oculi,
pars palpebralis, and corrugator supercilii are sig-
niﬁcantly different, although these two muscles
share the same innervation and embryonic origin
and are found in the same region of the face (lower
eyelid and lower mid forehead, respectively). The
orbicularis oculi consists of 89% fast-twitch ﬁbers,
signiﬁcantly more than the corrugator, implying
some difference in the movements produced by the
two muscles (Goodmurphy and Ovalle, 1999). Zygo-
maticus major and zygomaticus minor muscles are
similar to the orbicularis oculi in their high propor-
tions of fast-twitch ﬁbers, relative to other muscles,
Contempt and embarrassment have also been proposed as univer-
sal facial expressions of emotion, with varying degrees of universality
in expression recognition reported (Haidt and Keltner, 1999).
Fig. 2. Eyebrow ﬂash of greeting (Eibl- Eibesfeldt, 1989).
FACIAL EXPRESSIONS AS ADAPTATIONS 5Schmidt and Cohn]
indicating a possible specialization for fast move-
ments (Stal et al., 1987).
There are also individual differences in the struc-
ture and differentiation of facial muscles. For exam-
ple, a differentiated muscle bundle, the risorius,
thought to be unique to humans, is highly variable.
As many as 22 of 50 specimens in a recent study
lacked this muscle (Pessa et al., 1998a), and Huber
believed that it was absent completely in people of
Melanesian ancestry, although this ﬁnding has not
been replicated (Huber, 1931). Various furrows and
other deformations of the facial skin are produced by
variations in facial muscles, and these may contrib-
ute to individual differences in expression. In most
individuals, the platysma muscle inserts on the skin
over the inferior margin of the mandible, but it is
occasionally observed inserting in the lateral cheek,
causing a vertical depression or furrow to appear
there. The zygomaticus major muscle also varies,
appearing in a biﬁd version with two separate inser-
tion points in 17 of 50 of specimens in an anatomical
study (Pessa et al., 1998a). The tension caused by
the two heads of the muscle at the corner of the
mouth is believed to cause a dimple or small depres-
sion during the contraction of the muscle in smiling
(Pessa et al., 1998b). Changes in facial texture, such
as dimples that appear with a smile in some indi-
viduals, could be of added value in making an ex-
pression noticeable, or in providing information
about the intensity of the expression.
A study of facial musculature in living humans
noted a signiﬁcant sex difference in the thickness of
the zygomaticus major muscle (McAlister et al.,
1998). This study also investigated differences in
musculature, and found no signiﬁcant differences in
either levator labii superioris or zygomaticus major
muscle thickness between Asians and Caucasians
(McAlister et al., 1998). In general, there is not a
great deal of published information on populational
or sex-based variation in facial muscles, and ﬁnd-
ings of populational differences described above
have not been replicated.
The effects of interindividual anatomical varia-
tion, including genetically based variation on facial
expression, are even less well-known. The muscles
themselves are highly variable, with some muscles
appearing in some individuals and not in others
(Pessa et al., 1998b). The presence of anatomical
variation raises important questions about the link
between facial actions and speciﬁc muscles. The re-
lationship between muscle activity and displace-
ment of facial features in expression is individual-
ized to some degree; during posed eyebrow raises,
muscle activity is roughly equal to brow displace-
ment squared. Yet there is wide variation for indi-
vidual brows and left brows rise higher, given the
same amount of muscle activity (Pennock et al.,
On the other hand, if the action of the face is the
same, although there is variation in the underlying
muscular structure, the resulting facial expressions
may not be meaningfully discriminated. The univer-
sal recognition of some basic expressions indicates
that facial expressions may not depend on a one-to-
one anatomical correspondence in any two facial
signalers. Basic facial expressions are also recogniz-
able in abbreviated form, without the complete set of
facial actions described for the prototype expression.
Regardless of the degree of variation that can be
detected empirically, perceivers may take no notice
of these slight variations (Fridlund, 1997; Shor,
1978), or may categorize them similarly, with high
agreement (Campbell et al., 1999; Cashdan, 1998).
More importantly, it is unknown whether such phe-
notypic variation in facial expression meets these
criteria of “just meaningful difference”(Hauser,
1996) by causing differences in receiver behavior or
judgment to slightly variant displays of the same
Variation in neural control of facial muscles
Neurobiologically, facial expressions are dually
controlled by extrapyramidal and pyramidal tracts,
providing for automatic and voluntary control of
Fig. 3. Muscles of facial expression. 1, frontalis; 2, orbicularis
oculi; 3, zygomaticus major; 4, risorius; 5, platysma; 6, depressor
anguli oris. Original drawing from Huber (1931). (Reprinted by
permission of The Johns Hopkins University Press.)
6YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 44, 2001
facial expression. Based on observations of individ-
uals suffering from various neurological conditions,
Rinn (1984) described both systems of facial move-
ment, along with the differential voluntary control
over upper and lower face, related to greater asym-
metry and voluntary control over the mouth region
than the eyes. This difference is especially apparent
in the facial expressions of people with cortical vs.
extrapyramidal deﬁcits. Those lacking cortical con-
trol produce largely asymmetrical voluntary (posed)
expressions, but symmetrical spontaneous expres-
sions. Extrapyramidal deﬁcits produce the opposite
effect (Rinn, 1984; Ross and Mathiesen, 1998).
Potential asymmetry due to differences in inner-
vation of sides of the face may be related to sex
differences in the brain, and therefore produce vari-
ation in facial expression among individuals. This is
especially true if increased lateralization of cortical
function in males includes more lateralized facial
movement during expressions (Richardson et al.,
2000). Spontaneity of expression also may play a
role, with more spontaneous facial expressions un-
der the control of a different neural pathway, and
therefore more symmetric (Gazzaniga and Smylie,
1990; Rinn, 1984).
Research has not clearly conﬁrmed the predictions
of Rinn (1984) for asymmetry in lower face motion,
especially in spontaneous expressions. Borod et al.
(1998), in a meta-analysis of facial expression and
asymmetry, concluded that facial expressions could
generally be considered left-sided. However, they
did not ﬁnd that men were more likely to have
asymmetry in their facial expressions, although in-
dividual studies had previously suggested this.
Other researchers, using more objective quantita-
tive methods (direct assessment of digitized images,
rather than observer judgments or observer coding)
found that the upper face was much more asymmet-
ric than expected, particularly during spontaneous
expression (Richardson et al., 2000).
In addition, the complex connections that have
been proposed between the experience of positive
and negative emotions and facial expression and
cerebral laterality are still in question (Borod et al.,
1998; Hager and Ekman, 1997). Borod et al. (1998)
found signiﬁcant left-sidedness of facial expression
in studies involving muscle quantiﬁcation and
trained observer ratings (38 of 66 total studies
showed left-sidedness as compared to 3 of 66 show-
ing right-sidedness). The evidence of right-sidedness
for positive expressions (smile), and left-sidedness
for other emotion expressions, was much weaker
(Borod et al., 1998). Although the role of asymmetry
in the quality of facial signals is not clear, asymmet-
ric facial expression is likely to be an important
variable in considering facial displays as adapta-
tions, particularly as it relates to spontaneity or
deliberateness of expression.
Asymmetry in facial display is also probably re-
lated to individual differences in structural asym-
metry that play a powerful role in our perceptions of
human attractiveness and mate quality (Thornhill
and Gangestad, 1994). Interestingly, most studies of
facial expression asymmetry do not take into ac-
count whether or not structural asymmetry or move-
ment asymmetry is responsible for asymmetry of
facial expression. It is possible that asymmetry in
expression is largely determined by asymmetries in
the structure of the face at rest (Smith, 1998). By
necessity, observer judgments of expression inten-
sity can only be collected from faces at the height of
expression, where both structure and movement
have played a role in generating asymmetry. Elec-
tromyographic (EMG) studies of facial expression
seem to support the idea that asymmetry in expres-
sion is simply a result of asymmetry in the structure
of the face, because similar amounts of muscle ac-
tivity are found on both sides of the face (Borod et
al., 1998). In at least one case, the differential effects
of similar muscle activity on facial features has been
demonstrated (Pennock et al., 1999).
In more indirect fashion, the evolved perceptual
preference for symmetry in structure may also ex-
tend to a preference for symmetry in movement.
Spontaneous smiles, for example, are more symmet-
ric than are posed smiles (Frank et al., 1993). They
are also considered more sincere and possibly more
Variation within facial expression
Universal facial expressions, though distinct, are
not uniformly produced or perceived. Asymmetry,
due to neurobiological constraints and the relative
spontaneity of facial movement, is one source of
variation, but there are many others. Part of the
difﬁculty is that expression has too often been stud-
ied opportunistically, without prior expectation or
theoretical outlook on why particular facial move-
ments should be grouped, or how the display as a
whole came to be in the ﬁrst place. Smiling is a good
example of this problem. For example, smiling or the
joy display typically involves upturned lip corners,
and may also involve the squeezing and wrinkling of
skin around the lateral corner of the eye (orbicularis
oculi). Smiles that include both orbicularis oculi and
zygomaticus major activity have been called Duch-
enne smiles in honor of the French anatomist, while
smiles lacking orbicularis oculi activity are non-
Duchenne smiles (Frank et al., 1993). Smiles also
vary in their intensity, in the associated activity of
other facial muscles such as frontalis, and in the
open or closed position of the mouth (Blurton Jones,
1972; Cheyne 1976; Jones et al., 1990; Messinger et
al., 1999) (see Figs. 4, 5). The signiﬁcance of open or
closed mouth smiling is also unknown, although dis-
cussions of nonhuman primate and human homol-
ogy in expression suggest an appeasement function
for closed bared teeth displays (smiles) and a play
readiness function for open mouth displays (laugh-
ter and open mouth smiling) (Preuschoft, 1992; van
FACIAL EXPRESSIONS AS ADAPTATIONS 7Schmidt and Cohn]
Although the anatomical basis of facial expression
in general is fairly well-established, important ques-
tions about the timing and patterning of facial move-
ment also remain unanswered. Spontaneous enjoy-
ment smiles appear to function within time
constraints, typically lasting between 0.5–4 sec and
having smoother transitions between onset, apex,
and offset of movement (Frank et al., 1993). In a
study of adult women’s smiles toward children, var-
ied onset and offset timing of smiles were differen-
tially interpreted by child observers. Smiles with
relatively quicker offset periods were interpreted as
less genuine by these children. Individual adult dif-
ferences were found in patterns of onset and offset
timing of smiles, and approximately 16% (122 of
763) of these smiles had multiple peaks, reinforcing
the difﬁculty in assessing the temporal course of a
smile (Bugental, 1986). Using a quantitative mea-
sure of change in smile appearance, Leonard et al.
(1991) found that observers perceived the maximum
difference in levels of happiness within the same few
frames in which the smile changed the most. They
interpreted the temporal change in smile, typically
occurring within in a 100-msec window, as a tem-
plate for smile perception. This timing may corre-
spond to the limits of the perceptual system (Frid-
lund, 1994), and is remarkably similar to the timing
of onset in the spontaneous eyebrow ﬂash (Grammer
et al., 1988). Speed of smiling (and possibly other
expressions) is likely a feature of both expression
Also of interest are the patterns of coordinated
movements occurring during expression. In the case
of the eyebrow ﬂash, the apex of the expression is
also relatively stable, unaccompanied by the appear-
ance of new facial movements (Grammer et al.,
1988). This suggests that even for the very mobile
and ﬂexible human face, there may be limits on the
types and time course of spontaneous expressions.
Head and eye movements may also occur during
facial expression, and are probably coordinated with
facial movements, as components in a multicompo-
nent display (Ekman, 1979; Niemitz et al., 2000).
Lyons et al. (2000) demonstrated that head position
has signiﬁcant effects on the perception of facial
expression; head position changes were perceived as
facial expression changes, even in the absence of
facial muscle activity.
Given the great diversity of human facial expres-
sion, anthropologists tend to note the ﬂexibility,
complexity, and voluntary nature of facial expres-
sion (Birdwhistell, 1970). Compared even to rela-
tively expressive nonhuman primates, like chimpan-
zees, human facial expression seems to be too
variable to be divided into well-deﬁned phenotype
sets. Voluntary control over facial muscles, espe-
cially over the muscles of the mouth, is a hallmark of
human nonverbal expression, and is likely due to
the articulatory demands of human language (Rinn,
1984). The diversity of voluntary and spontaneous
human facial expression, however, should not be
mistaken for inﬁnite variability in facial expressions
as actually performed. Current research on the con-
ﬁguration and temporal course of facial expression
seems to support this idea, as it has so far shown a
great degree of regularity in expression across cul-
tures and individuals.
Individual differences in observable facial
In addition to underlying physical variation in the
face and in movement, empirically measured facial
behavior varies according to factors such as sex
(Briton and Hall, 1995; Chapell, 1997), age (Chapell,
1997), and cultural background (Ekman, 1973; Kup-
perbusch et al., 1999). Also important in facial ex-
pression are individualized factors, such as sociality
of situation (Fridlund, 1994; Friedman and Miller-
Herringer, 1991; Jakobs et al., 1999) and the emo-
tion-eliciting nature of visual or other stimuli (Cohn
and Tronick, 1983).
Humans vary in their ability and tendency to pro-
duce facial expressions, and this variation is pre-
sumably related to underlying muscular, neurobio-
logical, or social differences. Nevertheless, variation
in the signal itself, the visible changes in the face, is
important to addressing hypotheses of the signaling
value of facial expressions. Dimensions of nonpatho-
logical variability include interpersonal success in
nonverbal communication (Strahan and Conger,
1998) and overall expressiveness (DePaulo, 1992).
There are also sex differences in facial expression,
especially for smiling, with women smiling more
(Briton and Hall, 1995; Chapell, 1997; LaFrance and
Hecht, 1999). LaFrance and Hecht (1999) maintain
that women are not comfortable unless they are
smiling. Women have also been shown to have
thicker zygomaticus major muscles, although it is
unknown whether this is a cause or consequence of
increased smiling (McAlister et al., 1998). Sex dif-
ferences in facial expression are not only frequency-
based, however; there is also some evidence that
women specialize in expressions of happiness, while
men are better performers of angry expressions
(Coats and Feldman, 1996). Individual differences in
Fig. 4. Non-Duchenne and Duchenne smiles. a: Non-Duch-
enne smile. b: Duchenne smile. Images from Kanade et al. (2000).
8YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 44, 2001
facial expression may be apparent even in neonates
(Manstead, 1991). Most of these results are from
industrial societies, and therefore, the range of hu-
man variation is probably not fully represented. Yet
behavioral phenotypes, including universal expres-
sions and facial displays, are clearly variable.
Methods in facial expression research
Hauser (1996) stresses the importance of methods
that allow rigorous comparison among studies of
communication. Currently, there are relatively few
detailed objective methods, although recent work in
facial expression research holds promise for im-
proved expression analysis. The development and
use of the Facial Action Coding System (FACS), an
anatomically based coding system for recording ap-
pearance changes caused by the action of individual
muscles, was the ﬁrst to make possible the collection
of a large body of reliable empirical data on these
expressions (Ekman and Friesen, 1978; Ekman and
Rosenberg, 1997). New methods of facial measure-
ment allow even more objective, quantitative mea-
surement of facial movement (see Fig. 5). Automated
versions of FACS, which will automate the process
of studying facial action, are currently being devel-
oped (Cohn et al., 1999). Other automated methods
have been used for studying nonverbal signals in
general (Grammer et al., 1999), and facial expres-
sions in particular (Richardson et al., 2000; Scriba et
al., 1999). These methods rely mainly on overall
change in images of the face (or entire body) over the
course of nonverbal expression. Amounts of change
in the image, assuming all images are collected in
the same manner, are interpreted as movement pat-
terns (see Fig. 5).
Phenotypic variation in facial perception
Along with the study of the neurobiological and
anatomical and behavioral aspects of facial action,
the perceptual aspects of face recognition and facial
expression recognition have also received a great
deal of attention in the past several decades. In
proposing that patterns of facial movement are com-
municative adaptations, there is also the task of
understanding the coevolution of perceptual mecha-
nisms (Chovil, 1997; Endler 1993; Fridlund, 1997;
Fig. 5. Automated method for quantifying facial movement. a: Posed smile with outlined features tracked automatically (Tian et
al., 2001). b: Movement (radius length relative to mouth center) of right and left lip corners calculated from positional change in
tracked features over ﬁrst 400 msec of expression (Schmidt and Cohn, 2001).
FACIAL EXPRESSIONS AS ADAPTATIONS 9Schmidt and Cohn]
Hauser, 1996). There is good evidence that neurons
in particular areas of the brain have speciﬁc sensi-
tivity to social stimuli, including but not limited to
static faces. The primary evidence for the existence
of separate neurobiological mechanisms of facial ex-
pression recognition comes from studies of disso-
ciable deﬁcits: the ability to recognize faces is re-
tained, while the ability to recognize expressions is
lost in brain damage (Ellis and Young, 1998; Young
et al., 1998) or in cases of autism (Celani et al.,
1999). This evidence supports a theory of neurobio-
logical specialization for social stimuli (Adolphs,
1999; Brothers et al., 1990).
Facial expressions are processed by several dis-
tinct brain regions. The amygdala is largely re-
sponsible for perception of fear and sadness ex-
pressions. Some researchers suggest that the
amygdala may in fact be specialized for perception
of fearful expressions only (Morris et al., 1996).
Other regions, including the somatosensory and
orbito-frontal cortex, are involved in recognizing
emotion blends and anger (Adolphs, 1999; Blair et
al., 1999; Morris et al., 1996). The difference be-
tween explicit processing (subjects instructed to
judge facial expressions) and implicit processing
(subjects instructed to judge sex of actor) may
affect the region of brain used for processing, with
implicit processing handled largely by the amyg-
dala (Critchley et al., 2000).
Differences in facial expression processing likely
relate to differences in adaptive behavioral re-
sponses to expressions. For example, Dimberg
(1997) found that conditioning to faces worked much
better for fear than for any other expression. Neu-
robiological specialization for facial expression pro-
cessing also corresponds to the suggestion that per-
ception of certain signals requires greater
sensitivity (perception of anger at very low levels is
likely to give a ﬁtness advantage; Gosselin et al.,
While the variation inherent in neurobiological
perceptual systems is unknown, there is evidence for
individual differences in facial expression percep-
tion. The most striking ﬁnding is that women appear
to be more accurate and more sensitive decoders of
facial expression than men, and that this ability
develops in children as young as 3 years (Boyatzis et
al., 1993; Hall, 1984; McClure, 2000). Women in one
study gave higher ratings than men did to happy
expressions and lower ratings to neutral expres-
sions, suggesting they differentiate more among fa-
cial expressions of varying intensities (Katsikitis et
al., 1997). Otta et al (1996) also found slightly
greater discrimination among women, as perceivers
A more speciﬁc ability, detection of deceit, also
varies among individuals, and appears to be based
on a more widely applicable ability—being able to
detect small, extremely rapid changes in facial ex-
pression (Frank and Ekman, 1997). This ability to
detect subtle changes in facial movements may also
be an important individual difference. For example,
some people were better able to judge smiles of en-
joyment accurately, especially those who paid more
attention to the eye region (Frank et al., 1993).
Finally, cultural background plays an important
role in the attribution of personality traits to partic-
ular facial expressions. People with smiling faces
are interpreted as more sociable than people with
neutral faces by both Japanese and American sub-
jects. However, the difference between the sociabil-
ity of neutral and smiling faces is much higher for
Americans than it is for Japanese subjects (Matsu-
moto and Kudoh, 1993).
Diversity among facial expression phenotypes
Although the concept of basic universal expres-
sions has allowed us to consider human facial ex-
pressions as evolved behavioral phenotypes, an em-
phasis on universality obscures the abundance of
variation within and between facial expressions. All
facial expression phenotypes are not created equal.
For example, some expressions are produced much
more often than others (smile; Bavelas and Chovil,
1997), as frequently as two or three separate dis-
plays per minute of face-to-face interaction
(Schmidt, 2000). Others, such as the Duchenne
smile and the fear expression, cannot be as easily
produced voluntarily. Some are quite infrequent
and/or may not be as universally recognizable as
others (disgust, fear, contempt; Fridlund, 1994). Dif-
ferent expressions are also associated with speciﬁc
variation in autonomic functioning, suggesting dif-
ferent roles in emotional, self-regulatory processes.
For example, fear expressions increased heart rate
and sadness expressions decreased it (Levenson et
Even expressions that seem superﬁcially simi-
lar, such as smiling and laughing (to be discussed
later), are now best studied as separate pheno-
types, given our current knowledge of their forms
and functions (Keltner and Bonanno, 1997;
Preuschoft and van Hooff, 1995; Provine, 1996,
1997). Smiling typically bares the teeth, but does
not necessarily involve vocalization, unlike laugh-
ter, which has a characteristic pattern of open
mouth and exhalation/vocalization associated
with it, and may also include repetitive eye and
mouth closure patterns (Niemitz et al., 2000). Ex-
tensive variation both among and within facial
expression phenotypes clearly requires multiple
adaptive explanations, rather than a single hy-
pothesis of facial expression. The ﬁt between be-
havioral phenotype, ecological context, and ﬁtness
consequences for facial expressions is speciﬁcto
each particular expression phenotype. In general,
however, facial expressions can be considered so-
cial signals, which is a good starting point from
which to diverge into multiple adaptive contexts.
10 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 44, 2001
ECOLOGICAL CONTEXTS AND FITNESS
Facial expressions as social signals
Facial expression is unambiguously social, in that
the expressions are produced with greater frequency
and intensity in social situations and can be directly
linked to interactive consequences (Fridlund, 1994;
Jancke and Kaufmann, 1994). If facial expressions
(including displays of emotion) are social adapta-
tions, then they are signals, produced primarily with
a social purpose. Whether or not emotion is associ-
ated with most facial expressions, or even any facial
expression, is an issue of great importance in the
psychology of emotion. If facial expressions are sim-
ply outward expressions of emotion, and there is no
speciﬁcﬁtness consequence proposed for the expres-
sions themselves, then they are subject to other
levels of analysis. When facial expressions are con-
sidered as potential adaptations, however, the rela-
tionship between experience of emotion and expres-
sion is not necessarily relevant (Hauser, 1996;
although see Keltner and Gross, 1999, for a func-
tional hypothesis of emotions in general). Forming
hypotheses about the adaptive nature of facial ex-
pressions as social signals requires only that speciﬁc
ecological contexts and ﬁtness consequences of these
behaviors be described. Adaptive explanations of the
signals themselves may or may not include adaptive
explanations of human emotions that underlie much
of facial expression.
Because they occur largely in the interactive con-
text, human facial expressions are generally consid-
ered to be cooperative signaling systems, beneﬁting
both signaler and receiver (Fridlund, 1997). Al-
though it is not generally discussed, facial expres-
sions can probably be considered low cost, as the
energy required to produce an individual spontane-
ous expression is small. Such low-cost, frequent sig-
nals are expected in mutually beneﬁcial interactions
(Krebs and Dawkins, 1984), or within groups of re-
lated individuals (Bergstrom and Lachmann, 1998).
Facial expressions, however, occur in many differ-
ent social contexts, not all of them cooperative. The
complex relationships between social contexts and
shared and conﬂicting interests suggests that hu-
man facial expressions have multiple signaling func-
tions. As extensive modeling, and some empirical
work in nonhuman primates has shown, the ecolog-
ical contexts and ﬁtness consequences of behavior
are critical in determining the nature of the signals
that evolve (Godfray and Johnstone, 2000; Grafen
and Johnstone, 1993; Krebs and Dawkins, 1984).
Socioecological contexts of human facial
Human ecological contexts are undeniably socio-
ecological contexts. Even nonsocial contexts may be
framed in social ways, because of past selective pres-
sures on the design of the mind (Brothers, 1997;
Humphrey, 1976; Kummer et al., 1997). Absent or
semipresent individuals provide enough social con-
text to produce facial expression (speaking with
someone on the phone, or knowing a friend is doing
the same activity in the next room; Fridlund, 1994).
These types of contexts are, of course, unlikely to
have been important until recently in our evolution-
ary history, but they illustrate our readiness and
willingness to produce facial expressions at even the
suggestion of social interaction.
Humans are not completely unresponsive in the
absence of social partners, but facial expressions
vary in their susceptibility to audience effects, with
changes in frequency and/or type of movement with
different receivers (Jancke and Kauffmann, 1994;
Kraut and Johnson, 1979). Some expressions vary
little along social dimensions (startle), while others
vary signiﬁcantly (smile). For example, Fridlund
(1994) and others have found that smiling decreased
monotonically with decreasing social contexts (view-
ing a tape with a friend, viewing a tape that a friend
is watching in the next room, viewing a tape while
friend is off completing tests, viewing a tape alone).
The knowledge that a friend was performing the
same task led subjects to smile signiﬁcantly more.
Kraut and Johnson (1979) observed a similar phe-
nomenon among bowlers, who smiled at friends
more often than they smiled at a spare or strike.
Hess et al. (1995), Jancke and Kaufmann (1994),
and Manstead et al. (1999) found similar effects of
sociality, concurrent with the effects of emotion-elic-
iting stimuli. Obviously, the natural context of facial
expression is social interaction, and anthropological,
adaptive explanations of facial behavior require at-
tention to speciﬁc, naturalistic ecological contexts.
This type of approach has been suggested by
Preuschoft (2000) with respect to the positive emo-
tions, and could be adapted for the positive facial
expressions of emotion. She includes several con-
texts for recategorizing the positive emotions, in-
cluding interacting with babies, interacting with
others playfully, seeking mates, and other social
contexts. Bradbury and Vehrencamp (1998) sug-
gested a similar list: conﬂict resolution, territory
defense, sexual signals, parent/offspring interaction,
social integration, environmental contexts, and au-
In this paper, we propose the following set of so-
cioecological contexts for a beginning exploration of
facial expression as adaptation: infant/caregiver in-
teraction, cooperative interactions, speech, and in-
traspeciﬁc competitive interactions. We consider
Adaptive explanations of facial expressions as emotions are based
primarily on the adaptiveness of experiencing emotions. Expressing
emotion is an important part of signaling hypotheses of expression.
The exploration of relationships between internally experienced emo-
tion and facial expression is an important part of adaptive hypotheses
of emotions, but the link between expressions of emotion and ﬁtness
consequences does not necessarily require that other adaptive conse-
quences of that emotion be explained.
FACIAL EXPRESSIONS AS ADAPTATIONS 11Schmidt and Cohn]
each separately deﬁned ecological context as a
source of variation in costs and beneﬁts of facial
signaling, with separate ﬁtness consequences for
Both cooperative and competing interests of care-
givers (parents) and offspring are probably reﬂected
in the signaling systems that develop in the context
of this interaction (Trivers, 1974). Infants may pro-
duce honest signals of need (Grafen, 1990; Godfray
and Johnstone, 2000). Another possibility is that
infant signals of need are exploitative, or represent
the outcome of sibling conﬂict (Godfray and John-
stone, 2000). Infant facial expressions can be inter-
preted in these signaling contexts.
Infants display basic facial expressions that are
similar to or the same as those of adults (Fig. 1).
Some of the component movements of facial expres-
sion are probably innate (Izard and Malatesta, 1987;
Meltzoff, 1996). In addition, studies of infant facial
expression are most accessible to adaptive perspec-
tives, in that researchers are unable to rely on self-
report and must instead look at expression ethologi-
cally and with an eye toward consequences of
Human infant displays have been discussed in the
literature from a signaling perspective. Infant cry-
ing is generally interpreted as an honest signal of
need, as expected theoretically (Fridlund, 1997;
Hauser, 1996). Facial expressions associated with
crying are part of this multicomponent signal, and
crying is effective in getting attention.
Infant smiling as a display is also coordinated
with caregiver behavior. Infants look at their moth-
ers whether the mother is attentive or not, but they
only give the signal (smile) if she is attentive (Jones
et al., 1991). The probability that an infant will
smile at its mother is greatest when the mother is
most attentive and also smiling (Cohn and Tronick,
1987). Infant bouts of smiling end quite abruptly
when the mother ceases smiling (Cohn and Elmore,
1988). These results suggest that infants’production
of smiles is sensitive to the potential costs and ben-
eﬁts of making this expression. Since infants are
subject to both maintenance and growth needs, they
could be expected to modify even these seemingly
inexpensive signals, depending on the potential for
positive response. Positive responses, in this case,
would be directly related to positive ﬁtness conse-
quences, including increased opportunities to inter-
act, leading to earlier and better performance in
social interaction. The function of infant smiling and
mother infant interaction in the development of se-
cure attachment is also signiﬁcant in that secure
attachment in infancy has been demonstrated to
predict social competence later in childhood, while
insecure attachment has negative consequences
(Belsky and Nezworski, 1988).
One of the positive consequences of facial expres-
sion seems simply to get attention focused on one-
self. Faces and facial expressions draw attention
(Vuilleumier, 2000). Much of the work on this most
simple effect of facial expression comes from the
study of infant interaction. Human infants use facial
expression to induce their mothers to pay attention,
and mothers typically vocalize or smile in response
(Jones et al., 1990). The bared teeth smile seems
particularly useful in this context; Jones et al. (1990)
found bared teeth smiles are more likely to be pro-
duced in social situations, when the infant is paying
attention to its mother and not to toys. These bared
teeth smiles subsequently elicit responsive and at-
tentive behavior from the mother, a positive ﬁtness
consequence. The ﬁtness effects of parental atten-
tion for the human infant are potentially great, con-
sidering the intense social and nutritional needs of
the infant, as well as possible risks associated with
lack of maternal attention, including failure to
thrive, physical danger, and at the extreme, death
from neglect or abandonment. Whether or not these
social signals are honest signals of need or not, how-
ever, is difﬁcult to assess given our current knowl-
edge of infant smiling and attentional needs. The
relationship between infant facial expressions and
honest signals of need could be investigated, if need
were operationalized as continuing ﬁtness costs
(length of time since last feeding, distance from
mother, presence of sibling competitors), and signal
intensity and frequency were operationalized for
As infants develop, they more often initiate bouts
of smiling (Cohn and Tronick, 1987). They coordi-
nate facial displays with their caregivers (parents),
signaling only in what are considered appropriate
contexts. This coordination of signals may represent
a coordination of interests among healthy offspring
and healthy parents (those with incentive to con-
tinue investment). Among older children, it becomes
apparent that ability in sending and receiving facial
signals varies, and is associated with positive ﬁtness
consequences of personal and social adjustment
(Nowicki and Duke, 1994). As children get older,
they use their perceptions of smiles to ﬁne-tune
their expressions until their deliberate posed smiles
are relatively indistinguishable from their sponta-
neous smiles. There is strong evidence that this
process relies on visual observation. Deliberate
smiles of blind children were distinguishable from
their spontaneous smiles, when viewed by untrained
observers, while those of sighted children were not
(Castanho and Otta, 1999). As adults, persons blind
from birth produce voluntary expressions of emotion
that are signiﬁcantly less recognizable than those of
sighted individuals (Galati et al., 1997).
The specialization for infant signals of need is also
speciﬁc to target receivers of the signal. Infants vary
their signals, depending on the parent (Forbes et al.,
2000). Infant signals are differentially perceived by
men and women, and infant smiles increase accu-
racy in infant recognition in women only (Jones,
1984). Jones (1984) suggested that the smile was a
12 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 44, 2001
signal speciﬁcally directed toward women. Infants
may vary signaling, based on experience of in-
creased beneﬁts for the behavior. For example, in
infant smiling during parent/infant interaction, in-
fants often begin with a non-Duchenne smile and
then convert this smile to a Duchenne smile, by
adding the contraction of the orbicularis oculi
around the lateral edge of the eye (60% of all infant
Duchenne smiles observed; Messinger et al., 1999).
It is not inconceivable that this change in expression
could be related to dynamic changes in the infant’s
perception of beneﬁts of the energetically more ex-
pensive Duchenne smile.
Long-term cooperative social interaction
Infants’and children’s competence in producing
and perceiving facial expressions eventually devel-
ops into adult skill at using facial expression with
peers and other members of the social group. Rela-
tionships among relatives and other group members
are characterized by speech and also by extensive
facial expression behavior. The complexity of rela-
tionships in these groups means that contexts for
facial expression will vary from interaction to inter-
action, on a frequent basis.
Because of their unusual stability and tendency to
involve long-term relationships, human groups are a
likely context in which reciprocal altruism can de-
velop (Trivers, 1971). Reciprocal altruism would
clearly be greatly facilitated by the use of signals for
willingness to reciprocate or negative sanction of
failure to reciprocate. It is in this context of repeated
long term interactions that patterns of repeated fa-
cial expression can provide interactants with exactly
the information they need with regard to others’
intentions, altruistic or otherwise (Brown and
Moore, 2000; Silk et al., 2000). Brown and Moore
(2000) hypothesized that in some cases, an “altruist
detector”might be more valuable than a “cheater
detector”mechanism. Presumably this detector
would depend on input from stimuli such as facial
expression, tone of voice, and other nonverbal sig-
nals. In this context a conventional signal of rela-
tively small magnitude, but repeated performance
would be predicted (Dawkins, 1993). If a pattern of
signaling that corresponds with reliable altruism
can be maintained, then the pattern could become
ritualized as a representation of the sender’s altru-
istic intent. Continuous performance of this expres-
sion pattern might indicate that others can rely on
the actor to act in an altruistic fashion. Zahavi
(1993) notes that these types of reliable conventional
signals can work in the following way: “a signal
which seems to be performed alike by all individuals
in a set is in fact a ‘standard’against which the
quality of different individuals of the same set is
judged”(Zahavi, 1993, p. 228).
This explanation of facial expression in coopera-
tive interaction is congruent with the suggestion by
DePaulo (1992) that the primary goal of facial ex-
pression, conscious or unconscious, is self-presenta-
tion. According to DePaulo (1992), although decep-
tion could be adaptive, people are not trying to make
themselves appear as something they are not. In-
stead, people typically try to enhance the accuracy of
qualities they already display (DePaulo, 1992;
Schmidt et al., 2000). For positive facial expressions,
in particular, it could be proposed that they are
trying to appear more altruistic (Brown and Moore,
Several human facial expression patterns support
this view of altruistic signaling. Social status in
housemates was associated with smiling, with high
status housemates smiling more (Cashdan, 1998). A
closed mouth bared-teeth display in nonhuman pri-
mates is typically interpreted as a submissive or
appeasement display (van Hooff, 1972; Preuschoft,
1992; and see discussion below). This kind of display
is not expected to be most frequent in the highest
status individuals. However, another perspective,
based on cooperative signaling, could explain these
data. The individuals with high social status could
be signaling their high potential for, or willingness
to reciprocate (Brown and Moore, 2000). In fact,
smiling in this study was quite frequent, for both
males and females (smiling about 10% of the time
they were observed; Cashdan, 1998).
Grammer et al. (1988) found a similar frequent
signaling pattern in eyebrow ﬂashes, with the added
point that initial eyebrow ﬂash was typically the
most intense (getting attention of partner), followed
by conversational eyebrow ﬂashes (regularly signal-
ing to attentive partner; Grammer et al., 1988).
One problem with this explanation is the possibil-
ity of nonreciprocators using repeated low-cost con-
ventional signals, such as smiles, in a deceptive
manner. Then somehow these repeated signals must
be costly, or at least so costly as to negate the beneﬁt
for a cheater that uses them correctly, but decep-
tively (Zahavi and Zahavi, 1997). Or the signals, if
cheaply produced, could represent coordinating ac-
tivity among individuals whose interests are some-
times in conﬂict, but who beneﬁt by coordinating
activities nonetheless (Silk et al., 2000).
A signal has to truthfully represent the interac-
tant’s intentions to reciprocate: honest signals are
hard to fake (Keltner and Bonanno, 1997). An auto-
matic, nonconscious response (electromyographi-
cally measured response of the receiver’s own facial
muscles) to the smiling of others, occurs only to
Duchenne smiles that are more energetically expen-
sive and harder to fake (Surakka and Hietanen,
1998). A similar response occurs to the nonverbal
vocal components of speech. The corrugator muscle
activated in the case of anger, and the orbicularis
oculi muscle activated when hearing contented
voices (Hietanen et al., 1998). Contrary to Fridlund
(1997), these reﬂexive displays of emotion may be
quite adaptive, especially in contexts where auto-
matic, quick response is critical. Emotional readout
can be a powerful social tool, especially if it brings
about positive ﬁtness consequences for senders and
FACIAL EXPRESSIONS AS ADAPTATIONS 13Schmidt and Cohn]
receivers. For example, facial expressions play a role
in creating and supporting empathy, an emotional,
yet also adaptive phenomenon (Brothers, 1989;
Buck and Ginsburg, 1997; Keltner and Bonanno,
1997). Other positive ﬁtness consequences could in-
clude the likelihood of receivers sharing food and
other resources with the signaler, beneﬁts that arise
from the reciprocally altruistic relationship in gen-
The predicted characteristics of spontaneous
smiles in the context of long-term cooperators, there-
fore, include honest signals such as the Duchenne
sign (orbicularis oculi activity) and characteristic
timing (see Fig. 5). We know that spontaneous
smiles differ in quality, with more simultaneous
muscle actions that are more coordinated, as com-
pared to deliberate, posed smiles (Gosselin et al.,
1997; Hager and Ekman, 1997; Hess et al., 1995).
The contrast between Duchenne and non-Duchenne
smiles is often interpreted as the difference between
truly felt and less than sincere expressions of emo-
tion. Ekman and Friesen (1982) maintain that the
Duchenne smile is not easily faked, although a da-
tabase of 105 posed smiles contained as many as
67% Duchenne smiles (Kanade et al., 2000; and see
Fig. 4). Whether or not the signal can be faked, it is
still consistent with an adaptive signal hypothesis of
smiling. More honest signals tend to be more costly
signals, and the Duchenne smile, to the extent that
it is more sincere, is certainly more costly (involves
at least two muscles instead of just one; see Fig. 3).
In addition, Bugental (1986) found that longer, and
therefore more costly smiles, were interpreted as
more sincere. For laughter, Niemitz et al. (2000)
found that longer laugh expressions, with more dy-
namic eye and mouth movements, were judged to be
the most positive and sincere expressions by adult
The range of contexts under which spontaneous
smiles occur, and the resulting degrees of honesty
expected, have not been considered. More research
into the quality of nonverbal signals may be the key
to distinguishing expressions along a continuum
from more honest facial signals to those that are less
than sincere (Grammer et al., 1997). For example,
observer response toward spontaneous Duchenne
and non-Duchenne smiles from the same individual
would be predicted to differ, with the longest spon-
taneous Duchenne smiles generating the most pos-
Yet this perspective also suggests that even over-
learned or automatic signals, like the non-Duchenne
or “social smile,”could be important signals of coop-
erative intention, rather than emotion. If social
smiles are performed according to a regular pattern,
then signaling of positive intention could consist of a
regular pattern or script for signaling, and devia-
tions from the expected expression pattern would
signal negative intentions. Social smiles, and other
expressions, are coordinated and timed with atten-
tion to the listener. They typically occur as an alter-
nate response to verbal “back channels,”such as
“uh-huh”and “yeah,”that signal continued partici-
pation in a conversation (Bavelas and Chovil, 1997;
We propose a new perspective on the costs associ-
ated with these social signals. In addition to the
energetic costs of repeated signaling that add up
during a social encounter, there are signiﬁcant costs
to the signaler if he is to maintain the signaling
pattern properly. These costs are attentional. Tim-
ing requires attention, and attention requires the
redirection of the sender’s neural processing and
perception toward one interactant and away from
others. Only by paying attention to the receiver and
the course of the social interaction, can the sender
continue to signal correctly. The smile, for example,
is not a randomly performed signal. The small
amount of evidence available shows that smiling is
highly coordinated with the meaning as well as the
nonverbal aspects of speech. Smiling “too early”or
“too late”can cause an individual to appear insin-
cere (Bugental, 1986; Ekman and Friesen, 1982).
Smiling when the topic of speech prohibits smiling is
a signiﬁcant social faux pas.
For non-Duchenne smiling then, the cost of the
signal is the cost of the attention paid to the inter-
actant, rather than the added physiological costs
associated with a spontaneous Duchenne smile. This
prediction could be tested by observing the rate and
timing of social smiles and other facial expressions
during conditions in which attention is disrupted.
Alternatively, one could measure the loss of atten-
tion to outside events during a typical interaction, as
an approximation of the risk in focusing on one
individual while other potentially important events
or interactions are taking place. The level of involve-
ment in an interaction as measured by number or
intensity of social signals or gaze, among other mea-
sures, is predicted to correlate with decreased atten-
tion to other stimuli in the vicinity.
If regular signaling that one focuses on the
speaker is accomplished by smiling, then a violation
could be detrimental to individual ﬁtness. Self-pre-
sentation is arguably more important among poten-
tial reciprocators, i.e., people whom one already
knows. Regular smiling, then, could be a sign of
altruistic intentions and would be expected to be
more frequent around friends (Jakobs et al., 1999).
The social smile, with its high frequency, could be
the redundant signal that Johnstone (1997) pro-
poses is the best for getting across a message to
conspeciﬁcs. Krebs and Dawkins (1984) predicted
that cooperative signals should be small and rela-
tively inexpensive. An analysis of EMG or other
measure of facial exertion would be predicted to
show that this type of smile is much cheaper than
other expressions, like anger, fear, or disgust, which
corresponds with the fact that it is used frequently
in cooperative interactions.
14 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 44, 2001
Positive ﬁtness consequences
In proposing that smiling, or any other facial ex-
pression, is an adaptive social signal, it is important
to establish the positive ﬁtness consequences of such
a behavioral phenotype. There is evidence to suggest
that facial expressions function to increase coopera-
tion and afﬁliation during interaction. The positive
ﬁtness consequences of facial expression include the
promotion of social acceptance and afﬁliation, and
the moderation of the effects of socially negative
actions. While the effects of facial expressions, and
smiling in particular, have not typically been opera-
tionalized as ﬁtness consequences in the past, a
review of recent studies indicates that these conse-
quences are signiﬁcant, at least with regard to social
variables such as status. Smiling affects perception
of the smiler’s other important characteristics, by
increasing attributions of intelligence (Otta et al.,
1993, 1996), happiness (Otta et al., 1996), and social
status (LaFrance and Hecht, 1999). Although not
typically associated with grief, smile displays during
conversation, especially those that include orbicu-
laris oculi activity around the lateral edge of the eye,
increase perceiver sympathy for bereaved persons
(Keltner and Bonanno, 1997). People associate smil-
ing with happiness and with positive intentions di-
rected toward them (liking) (Floyd and Burgoon,
1999). Smiling, in both the United States and Japan,
is associated with increased sociability (Matsumoto
and Kudoh, 1993).
These responses are mostly determined by self-
report in psychological studies, but there is also
direct physiological evidence that facial displays can
bring about positive responses, even in the absence
of overt emotional response. For example, a study of
the effects of viewing Ronald Reagan’s reassuring
smile display (raised brows, tilted head, relaxed
open mouth smile) brought about physiological signs
of positive response, even in viewers who said they
did not support Reagan politically (Sullivan and
Clearly, smiling displays can bring about positive
ﬁtness consequences, and perhaps even convince
others of ones’willingness to reciprocate. There may
be some individuals who fail to signal regularly,
however. In this case, the failure to signal socially is
in itself a signal (Bergstrom and Lachmann, 1998).
The failure to smile correctly, or to produce an ap-
propriate level of facial expression during coopera-
tive social interaction, may be at the root of some of
the social difﬁculties of people with ﬂat affect as a
result of schizophrenia, Parkinson’s disease, and de-
pression, or facial paralysis (Mueser et al., 1997;
Sakamoto et al., 1997; VanSwearingen et al., 1999).
Signaling altruism also implies the presence of
remedial social signals. For individuals who fail to
act in an altruistic manner, and get caught, there
are also embarrassment and shame displays. Inter-
estingly, in embarrassment displays, there is also a
smile, although here it is interpreted as an appease-
ment signal (Keltner and Buswell, 1997). Shame
displays are slightly different, and do not typically
include a smile (Keltner, 1997). Although there is no
consensus on whether or not the smile is an honest
signal or not, the blushing response seems much
closer to the deﬁnition of an honest costly signal.
Also a component of the shame display, blushing
actually works, with signiﬁcant differences in the
perceptions of interactants depending on whether or
not an individual blushed. Blushing, which can be
part of a voluntary shame display including glancing
around and lowering the head, actually reduces neg-
ative evaluations of actor behavior (deJong, 1999).
As a remedial gesture, blushing may be particularly
potent, because it is a gesture that is generally be-
lieved to be impossible to fake. It is not surprising
then that it produces a better response in observers
than does the glancing around display, another re-
medial gesture (deJong, 1999). Keltner et al. (1997)
interpreted both shame and embarrassment dis-
plays as appeasement displays, and supported this
hypothesis with evidence that they are negatively
correlated with aggression in adolescent boys.
Facial expressions during speech
Facial expression during social interaction is pos-
sibly an honest signal of afﬁliation, or willingness to
reciprocate. Among humans, however, social inter-
action almost invariably involves speech, and there
are unique considerations in the adaptiveness of the
relationship between facial expression and speech.
Facial expression is coordinated with speech at sev-
eral levels: the use of muscles of facial expression to
articulate speech sounds (Massaro, 1998), the con-
tribution of facial expressions to the syntactic struc-
ture and meaning of particular utterances (Bavelas
and Chovil, 1997; Ekman 1979), and graded or qual-
itative conversational signals that apply to the over-
all meaning of speech (Ekman 1979).
In addition to its functions for the speaker, facial
expression is also an important part of listener ac-
tivity (as many as 20% of conversational expressions
were back channel cues, performed while the indi-
vidual was not talking; Bavelas and Chovil 1997).
Smiles are produced with the same timing as other
back channel conversational cues, such as “uh-huh,”
that signal continued participation in a conversation
(Brunner, 1979), and are also produced at the end of
utterances (Schmidt, 2000). Laughter occurs along
with speech in a coordinated pattern (Provine,
1997). Ekman (1979) detailed the multiple patterns
of association of brow movements with speech: as
“batons”stressing a particular word, as question
marks, or as “underliners”emphasizing a sequence
of words, among others. Although the role of facial
expressions and other gestures in language evolu-
tion may be limited, understanding the coevolution
of language and the “gesture-call”system is critical
to understanding human speaking behavior (Burl-
ing, 1993, with comment by Blount, p. 38 –39).
FACIAL EXPRESSIONS AS ADAPTATIONS 15Schmidt and Cohn]
Facial expressions might also be related to the
social functions of speech. Although humans prac-
tice some social grooming (Schievenhovel, 1997),
Dunbar (1996) suggests that the role of grooming in
human society has largely been taken over by con-
versation. If nonverbal signals, including facial ex-
pressions, are coordinated with speech, they might
also assist in the grooming function of speech. An-
drew (1962) notes that lip smacking and other lip
movements are intention signals for grooming in
nonhuman primates. It is also possible that humans,
while potentially “grooming”partners with speech,
have retained these intentional signals in the form
of lip sucking, lip wipes and lip biting (action units
28, 37, and 32, Ekman and Friesen, 1978). Fridlund
(1997) refers to lip biting as a sign of agitation, but
it may also be a sign of desire to groom which is often
is associated with agitation. It is an open question
whether or not these movements are more frequent
during “vocal grooming”than in other human social
Courtship and facial expression
Facial expressions are only a small proportion of
the large number of human courtship signals. They
are typically embedded in coordinated displays, in-
cluding both whole body and whole head move-
ments, as well as other signals. As such, they have a
role in signaling both interest and mate quality.
Signaling mate quality is accomplished by a number
of physical trait-based characteristics such as sym-
metry, glossiness of hair and skin, and healthiness
of eyes (Gangestad and Thornhill, 1997).
Because of the numerous available indicators of
potential mate quality, one might argue that facial
expression was unnecessary. However, it could also
be expected that facial expression would act in such
a way to enhance positive traits, while disguising or
concealing less positive traits (enhancing self-pre-
sentation as a potential mate). Eibl-Eibesfeldt
(1989) describes how clothing and makeup in many
cases, accomplish these goals, but facial expression
could provide an intermediate behavioral level be-
tween cultural modiﬁcation and physical, biological
The description of the courtship displays of young
German and Japanese women, for example, shows
the importance of both facial expression and other
nonverbal movements in signaling attraction (will-
ingness to mate or to consider mating). Grammer et
al. (1999) found that during mixed sex interactions
between young men and women, a woman’s interest
in her partner was related to the regularity of her
nonverbal signals. Smaller, more regular move-
ments in women’s nonverbal displays were associ-
ated with increased levels of interest (Grammer et
al., 1999). This could be the case for facial expression
as well. In the case of opposite sex interactants,
repeated signaling with honest signals could also be
interpreted as a sign of willingness to invest in a
mate, and therefore increase the likelihood of repro-
ductive opportunities for the signaler. While there is
little positive evidence to support this idea, there is
some negative evidence in that the lack of coordina-
tion of facial movements in people with schizophre-
nia can cause signiﬁcant social problems for people
with schizophrenia (Dworkin, 1992).
With regard to symmetry and mate selection, it is
possible that symmetric facial expressions (typically
spontaneous and difﬁcult to produce voluntarily)
evoke attractiveness in the same way that struc-
tural facial symmetry (also very difﬁcult to fake)
does (Gangestad and Thornhill, 1997; Grammer and
Thornhill, 1994). Finally, facial and other nonverbal
signals during courtship can be expected to be rele-
vant to other signals of mate quality and to coordi-
nate with them. The ﬂirtatious hair ﬂip (Grammer
et al., 1999), for example, shows dynamically the
quality of the hair, while open-mouthed expressions
may reveal the quality of the teeth, as well as the
tissues inside the mouth.
Strangers, competitors, and conﬂicts of interest
A variety of individual ecological contexts are in-
cluded here, mainly because of the general lack of
empirical information on facial expressions in these
different contexts. In contrast to previously de-
scribed situations, however, interactions with
strangers and other interactions where potential
conﬂicts of interest are likely to share some basic
Krebs and Dawkins (1984) suggest signals to
those whose interests potentially conﬂict with the
signaler should be stereotyped and clear, rather
than hidden. Facial expressions are expected to re-
vert to conventional forms that reveal as little extra
information as possible (Wagner and Lee, 1999). In a
classic study of Japanese and American students
responding to ﬁlms, facial expressions differ least in
the presence of an interviewer, demonstrating the
increased regularity of facial signals in a socially
risky situation (with interviewer, rather than alone;
Ekman and Friesen, 1978; Wagner and Lee, 1999).
Signalers have some conscious perception of their
signaling patterns: students can predict, based on
context, their own likelihood of smiling at a joke told
by a professor as compared to a joke told by another
student (Nagashima and Schellenberg, 1997). Ste-
reotyped nonverbal bodily displays are also charac-
teristic of interactions in which strangers meet
(Grammer et al., 1997).
The sender may modify normally beneﬁcial honest
expressions in these contexts, depending on poten-
tial costs or beneﬁts of revealing information. When
meeting strangers, humans sometimes attempt to
hide or suppress expression. For example, children
and young adults from a variety of cultures re-
sponded to a friendly stranger with a similar pattern
of direct gaze with expression, followed by hiding the
face, and then another glance (Eibl-Eibesfeldt,
1989). Concealment also occurs in competitive inter-
actions with known individuals. In a study of indi-
16 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 44, 2001
vidual differences of the tendency to self-monitor
facial expressions, some individuals were found to
conceal expressions of joy after winning. These
smiles were concealed either by covering with a
hand, or by twisting other muscles in the face into
positions that minimized the appearance of the
smile (Friedman and Miller-Herringer, 1991).
Yawns and laughs are also sometime concealed by
covering (Provine, 1997).
According to Fridlund (1997), concealment of emo-
tion is highly desirable, and coordinates with the
“dictate of privacy”in social interaction. This is mis-
leading, though, in that the desirability of conceal-
ment necessarily varies with the particular socioeco-
logical context. Only those facial signals that depend
on privacy between signaler and receiver for positive
consequences are expected to be concealed from the
rest of the group. Although there are likely to be
contexts in which people seek to hide their expres-
sions from others, facial expressions toward strange
conspeciﬁcs in many cases are expected to be clear
and easily readable, whether they signal internal
state or not (Endler, 1993).
Meetings between strangers represent an obvious
opportunity for deception, in that the altruistic ten-
dencies of the signaler are unknown to the recipient.
However, actively deceptive signals are expected to
disappear eventually, because they do not supply
the receiver with useful information (Zahavi and
Zahavi, 1997). Actively deceptive signals of this type
can be contrasted with concealment of basically hon-
est signals, as in the effective suppression of facial
expression in contexts where food resource, personal
reputation, or other positive outcome is at stake
(Ekman et al., 1997; Mitchell, 1999). A third strat-
egy, the modiﬁcation of internal states associated
with expressions (emotional states), may be the
most adaptive form of deception. Expressions gener-
ated under these conditions of self-deception would
then appear spontaneous and automatic (Alexander,
1987). Emotional readout is not necessarily an hon-
est signal: it may be the result of self-deception, and
so appear honest when it is not.
Various facial behaviors associated with deceit
have been described and tested empirically (Ekman,
1985; Ekman et al., 1997). These studies provide
interesting information on social intelligence and
Machiavellian intelligence in particular. However,
the same researchers also found that there is sub-
stantial variation in the ability of human observers
to detect these nonverbal signs of deceit. Although
some individuals have this capability, many, even
those with extensive experience or training (e.g.,
police ofﬁcers), are unable to reliably detect cheating
individuals using these cues (Frank and Ekman,
1997). In fact, at least for facial expression, human
cheater detection mechanisms seem to be remark-
ably bad at detecting cheating, at least among
strangers (DePaulo, 1992; Ekman, 1985; Gosselin et
al., 1997). Either these mechanisms do not provide a
clear ﬁtness beneﬁt, and have therefore not been
subject to selection pressure (Bradbury and Vehren-
camp, 2000; Zahavi, 1993), or else the relevant con-
text of cheater detection is found not among strang-
ers, but among social group members. Cheater
detection ability may depend on an almost statisti-
cal knowledge of the normal facial expression pat-
tern for a given interaction partner, rather than a
Cheater detection mechanisms are undoubtedly
an important feature in the evolution of human so-
cial intelligence, but in the case of facial expression
may not be very ﬁne-tuned (DePaulo, 1992). The
answer to these puzzling ﬁndings probably lies in
the structure of human social interaction, especially
in the distant past. Cheater detection would be ex-
pected for individuals with whom we have the most
contact (strangers would likely not have been
trusted in any case). We hypothesize that detection
of deception by observation of nonverbal behavior
may be limited to those individuals that have regu-
lar contact with the deceiver, and might not be ex-
pected anyway in those who have no prior knowl-
edge of this person (such as observers described in
Ekman, 1985 and Ekman et al., 1997). We are not
aware of any studies of the relative difference in
cheater detection performance based on the facial
expression of known and unknown subjects, but pre-
dict that cheater detection would be signiﬁcantly
better for known individuals.
If facial expressions are generally used as honest
signals, as part of an ordered sequence of actions
appropriate to a particular social context, relatively
infrequent use of these signals for deceitful purposes
is a possibility. Mitchell (1999) describes these reg-
ular sequences of events as social scripts, where
deception is dependent upon successful mainte-
nance of behavior patterns (including facial expres-
sions), that signal cooperation while individuals act
deceitfully in their own self-interest. For example,
the maintenance of friendly facial expression, fol-
lowed by negative actions toward others, constitutes
the deceptive use of a social script, facial expressions
associated with afﬁliative interaction.
Signal properties of facial displays
Facial expressions are usually thought of as inti-
mate, based in dyads such as parent/infant interac-
tions, or conversations. More attention, however,
needs to be drawn to the differential properties of
facial signals, such as their clarity across relatively
large distances (as far as 45 m; Hager and Ekman,
1979) and from angles other than directly face-to-
face. Although facial expressions are typically ob-
served at close range, their signal properties may
allow for accurate reading by individuals in the pe-
riphery (eavesdroppers). The detectability of signals
is an important factor in their ability to provide
positive ﬁtness consequences for signalers (Endler,
1993). A comparison between the distance of facial
expression recognition and average social distance
in other species would be interesting in this regard.
FACIAL EXPRESSIONS AS ADAPTATIONS 17Schmidt and Cohn]
The functions of facial expression
By using these adaptive frameworks, and clarify-
ing phenotype, ecological context, and ﬁtness conse-
quences of facial signaling, it becomes possible to
investigate facial expression from an evolutionary
perspective (Fridlund, 1994). Both social and emo-
tional expressive functions of facial expression can
be investigated from an evolutionary perspective
and represent different levels of analysis (Hauser,
1996, p.495; see Jakobs et al., 1999, for a discussion
of this issue from the psychological perspective). Fit-
ness consequences are particularly hard to detect,
especially given the cross-sectional nature of many
psychological studies of facial expression. A single
facial expression, with few exceptions, cannot be
expected to provide a dramatic ﬁtness beneﬁt or
cost. Rather, repeated signaling of intention or emo-
tion is probably the biggest contributor to ﬁtness
accruing from facial expression.
In addition, the critical factor in the ﬁtness of a
particular expression such as a smile may be the
difference between it and the average smile of the
actor. Psychological studies generally take a cross-
sectional approach, measuring only a few minutes of
expression in a large number of individuals. Longi-
tudinal studies of facial expression are few and far
between (but see Messinger et al., 1999). Still, we
can begin to get a picture of the importance of facial
expression to ﬁtness by considering some of the re-
sults of facial expression research.
PHYLOGENETIC PERSPECTIVES ON FACIAL
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 sig-
naling did not yet exist (Bradbury and Vehrencamp,
2000). Although these issues are theoretically im-
portant, the phylogeny of humans and the long pre-
history of sociality in the Primate order make it
somewhat unlikely that signaling with human facial
expression 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 alterna-
tive. In some cases, the amount of depression asso-
ciated with facial paralysis is directly related to the
degree of disability in producing a prototypical smile
(VanSwearingen et al., 1999). It remains to be dem-
onstrated, however, whether human facial expres-
sions function adaptively, or whether they are sim-
ply remnants of a prelinguistic past (Darwin, 1872/
Clearly, though, there are differences in the fre-
quency and intensity of facial expression across nor-
mal 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, depend-
ing on cultural and social context. Negative ﬁtness
consequences here are conceptualized as reduced
access to cooperative relationships that tend to en-
hance survival and reproductive potential. Given
the long history of sociality in our lineage and the
ubiquity of facial expression in observations of nat-
uralistic 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 behav-
ioral ﬂexibility. Production of basic facial expres-
sions, 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 expres-
Particular expressions, notably the silent bared
teeth and relaxed open mouth displays, have been
compared to the human smile and laughter (Cheva-
lier-Skolnikoff, 1973; Darwin, 1872/1998; Preuschoft,
1992; Preuschoft and van Hooff, 1995; van Hooff,
1972). Given the similar structure of the facial mus-
cles and adaptations for focusing on the face, homol-
ogy between 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 mon-
keys 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 different-
shaped muzzle (Preuschoft, 2000; see Fig. 6).
In addition, there are common neurobiological
bases among humans and other primates in the
control of facial expression. A recent study of projec-
tions from the cortex to the facial nerve nucleus in
rhesus macaques found a pattern similar to that
described by Rinn (1984). Bilateral cortical projec-
tions to facial nuclei control frontalis and orbicularis
oculi muscles, and contralateral projections to the
opposite facial nucleus, control the muscles around
the mouth, allowing hemispheric differences in ex-
pressiveness 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 mecha-
nisms of control also produce similar effects in non-
18 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 44, 2001
human primates. Hook-Costigan and Rogers (1998)
found that positive social calls and expressions of
marmosets were lateralized to the right, while neg-
ative social expressions (fear) were lateralized to the
left. Hauser and Akre (2001) also found that expres-
sions 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 left-
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 nonhu-
man 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 with
happiness has been called into question (Ekman,
1985; Fridlund, 1994). Nonhuman primate bared
teeth displays (as in Fig. 6) may be similar in mean-
ing and function to human smiles, depending on the
Human anger expressions and ape anger/fear ex-
pressions may also be homologous (Chevalier-
Skolnikoff, 1973). Embarrassment has been pro-
posed 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). Ho-
mology 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 non-
human 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 (Toma-
sello 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 embar-
rassment; see Provine (1997) for yawning. Humans
have the additional ability of hiding their expres-
sions with the actions of other facial muscles, espe-
cially around the mouth where the downward pull of
the depressor anguli oris muscle can somewhat con-
ceal the rise of the lip corners due to the action of
zygomaticus major (Ekman, 1985). Spontaneous ex-
pressions may have elements of concealment associ-
ated 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 in-
creased 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
Consideration of nonhuman primate facial expres-
sion, of course, is necessarily be speciﬁc to each
individual species. Divergent facial signaling sys-
tems, as well as some homology, are to be expected.
For the relationship between overall amount of ex-
pression and the structure of the facial nerve nu-
cleus, Peburn et al. (2000) found variation between
species, with the relatively more expressive ma-
caques (Macaca fascicularis) showing signiﬁcantly
larger and better deﬁned facial subnuclei than the
relatively less expressive patas monkeys (Erythroce-
bus patas). Aotus, the only nocturnal anthropoid,
has virtually no facial expression, and its facial mus-
culature is also relatively less differentiated (Chev-
alier-Skolnikoff, 1973; Huber, 1931).
Likewise, many features of human facial expres-
sion, although universal, are speciﬁc to our species.
The relative hairlessness of the human face, com-
pared to the majority of nonhuman primates, sug-
gests that the combination of exposed skin and re-
tained hair may have some signaling value. Brows
are an important component of human greeting and
surprise displays, as well as some smiles. Upturned
Fig. 6. Homologous displays in human and nonhuman pri-
mates. a: Rhesus macaque submissive display. Photograph by
Frans DeWaal, 1989.(Silent bared teeth display.) b: Human
smile. From Kanade et al.,2000. (Silent bared teeth display.)
c: Bonobo play face. Photograph by Frans DeWaal, 1988. (Re-
laxed open mouth display.) d: Human play face, from Forbes et
al., 2000. (Relaxed open mouth display.)
FACIAL EXPRESSIONS AS ADAPTATIONS 19Schmidt and Cohn]
inner brows also signal sadness or grief (Eibl-
Eibesfeldt, 1989; Ekman, 1979). Results of an in-
triguing study in which cross-species perception of
facial expression was tested, the brows, a highly
visible signal on the hairless human face, are not
used by macaques seeking to identify sad human
facial expressions. They rely instead on other, more
phylogenetically conserved traits, such as cheek
movement (Kanazawa, 1998). Retention of facial
hair in adult male humans may also play a role in
accentuating or concealing expression. Unfortu-
nately, there has been no research on male facial
hair as it relates to facial expression.
Functions of facial expressions in nonhuman
Like humans, many nonhuman primate species
pay close attention to the faces of other group mem-
bers. 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 and
unfamiliar conspeciﬁcs, and to categorize facial ex-
pressions of other chimpanzees (Parr et al., 1998,
2000; Parr and deWaal, 1999). Chimpanzees can
follow the gaze of another individual by paying at-
tention to its face (Povinelli and Eddy, 1996). Goril-
las, chimpanzees, and bonobos have all been re-
ported to monitor the gaze of others, in ways that
suggest they may be able to anticipate the impact of
their facial expressions on others’behavior (Mitch-
ell, 1999). Clearly, facial expressions are important
signals in the social lives of most nonhuman pri-
mates, just as they are for humans.
By monitoring facial expressions, the intentions of
others can be inferred. Because of their relatively
stable existence, social groups provide an environ-
ment in which low-cost, redundant signals can help
primates to keep track of the other individual, pos-
sibly similar to that which Chadwick-Jones (1998)
described for baboons. Cheater males may fail to
give continuous signals, and so must be monitored.
The failure to adhere to social scripts, including
facial expression patterns, draws attention to unco-
operative individuals (Mitchell, 1999). Groups of
nonhuman primates may also utilize redundant,
“cheap”vocal signals in order to coordinate their
activities (Silk et al., 2000). Haslam (1997) provided
a list of social grammars for primate interaction,
including communal sharing, authority ranking,
equality matching, and market pricing. These are
behavioral contexts of the type that could corre-
spond to functional variation in primate facial ex-
pression. As in humans, considering facial expres-
sions as adaptations would require speciﬁcation of
relevant phenotypes, ecological contexts, and posi-
tive and negative ﬁtness consequences.
Current functional approaches to facial expres-
sion are largely framed in terms of the proximate
functions of emotions associated with that expres-
sion (Keltner and Gross, 1999; Keltner and Haidt,
1999; Yik and Russell, 1999). Fridlund (1994) has
argued from a critical psychological perspective for
the consideration of all facial behavior in a behav-
ioral ecological or evolutionary framework. Evolu-
tionary approaches, however, are necessarily based
on the study of facial expressions as biological adap-
tations, and much of the recent work on facial ex-
pression has been conducted outside this perspec-
tive. Nevertheless, results from this type of
functional study of facial expression provide a basis
on which to base evolutionary hypotheses of facial
behavior. By detailing the phenotypic variation in
facial expression, clearly deﬁning the ecological con-
texts of facial expression, and describing some of the
positive ﬁtness consequences of these behaviors, we
have outlined an evolutionary approach to the study
of human facial expressions as adaptations.
By proposing testable hypotheses about the na-
ture of facial expression, we can also provide a ﬁrm
biological basis to other anthropological studies of
communication. The unfortunate, and probably un-
intended, view of nonverbal expression as represent-
ing an ancestral-primate primitive ability, while
language is uniquely specialized in humans, can
also be challenged from this perspective (Eibl-
Eibesfeldt, 1989). Instead of just assuming that non-
verbal expression has much in common with pri-
mate relatives, but is also culturally patterned, we
may be in a position to specify more clearly the
adaptive role of facial expression in human social
Human social intelligence is obviously a major
contributor to human brain evolution and intellec-
tual abilities. Our most specialized and adaptive
system of social signaling is human language
(Pinker, 1994). Remarkable in its complexity and
also because of its seeming discontinuity with non-
human 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 interac-
tion, and the positive consequences of these skills
are only now being described. This argues for in-
creased attention to the evolution of nonverbal sig-
naling systems, including facial expression, from the
perspective of physical anthropology.
We thank John S. Allen and Melissa Panger for
careful reading and helpful criticism of this article.
This research was supported by NIH grant MH12579
to K. Schmidt and by NIH grant MH56193 to J.
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