Resume : The importance of the
face in social interaction and social
intelligence is widely recognized in
anthropology. Yet the adaptive functions of
human facial expression remain largely unknown.
An evolutionary model of human facial expression
as behavioral adaptation can be constructed,
given the current knowledge of the phenotypic
variation, ecological contexts, and fitness
consequences of facial behavior. Studies of
facial expression are available, but results are
not typically framed in an evolutionary
perspective. This review identifies the relevant
physical phenomena of facial expression and
integrates the study of this behavior with the
anthropological study of communication and
sociality in general. Anthropological issues
with relevance to the evolutionary study of
facial expression include: facial expressions as
coordinated, stereotyped behavioral phenotypes,
the unique contexts and functions of different
facial expressions, the relationship of facial
expression to speech, the value of facial
expressions as signals, and the relationship of
facial expression to social intelligence in
humans and in nonhuman primates. Human smiling
is used as an example of adaptation, and
testable hypotheses concerning the human smile,
as well as other expressions, are proposed.
[...] PHYLOGENETIC PERSPECTIVES ON
FACIAL EXPRESSION
Homology in facial expressions Game
theoretic models of facial signaling assume the
actors have the alternative of not signaling at
all, and may refer to a past generation where
signaling did not yet exist (Bradbury and
Vehrencamp, 2000). Although these issues are
theoretically important, the phylogeny of humans
and the long prehistory of sociality in the
Primate order make it somewhat unlikely that
signaling with human facialexpression would
disappear completely in humans. This is
immediately apparent when considering the
drastic and deeply damaging social consequences
of facial paralysis (VanSwearingen et al.,
1999). These and other forms of complete facial
paralysis have such negative social consequences
that it is difficult to imagine the lack of
facial signaling as an alternative. In some
cases, the amount of depression associated with
facial paralysis is directly related to the
degree of disability in producing a prototypical
smile (VanSwearingen et al., 1999). It remains
to be demonstrated, however, whether human
facial expressions function adaptively, or
whether they are simply remnants of a
prelinguistic past (Darwin, 1872/ 1998).
Clearly, though, there are differences in the
frequency and intensity of facial expression
across normal individuals. Facial expressions
are not always produced when they would be
advantageous, and this may lead to negative
fitness consequences that are less dramatic than
those discussed above, but still potentially
costly in social interaction, depending on
cultural and social context. Negative fitness
consequences here are conceptualized as reduced
access to cooperative relationships that tend to
enhance survival and reproductive potential.
Given the long history of sociality in our
lineage and the ubiquity of facial expression in
observations of naturalistic social interaction,
we hypothesize that a certain level of facial
expression must be obtained, or the individual
risks losing the fitness benefits acquired
during earlier interactions.
The homology of human and nonhuman primate
facial expression may illustrate continuity
among facial expression phenotypes, especially
between apes and humans. Preuschoft and van
Hooff (1995) note the remarkable stereotypy of
facial expression across an order that is
usually known for its behavioral flexibility.
Production of basic facial expressions, such as
the fear grimace in rhesus macaques,also appears
to be highly canalized (Geen, 1992). It would be
surprising if the level of stereotypy and
homology in nonhuman primate expression did not
extend to at least some patterns of human
expression. Particular expressions, notably the
silent bared teeth and relaxed open mouth
displays, have been compared to the human smile
and laughter (Chevalier-Skolnikoff, 1973;
Darwin, 1872/1998; Preuschoft,1992; Preuschoft
and van Hooff, 1995; van Hooff, 1972). Given the
similar structure of the facial muscles and
adaptations for focusing on the face,
homologybetween nonhuman primate and human
facial expressions has been suggested (van
Hooff, 1972). The smile has been proposed as a
homologue to the silent bared teeth display
(SBT), and the laugh as homologue to relaxed
open mouth displays of monkeys and apes (van
Hooff, 1972; Preuschoft, 1992; Preschoft and van
Hooff, 1995). Preuschoft (2000) suggests that
the apparent contrast between the smile of
humans (upward lip corners) and the SBT of
nonhuman primates may simply be the result of
similar muscles stretched over a very
differentshapedmuzzle (Preuschoft, 2000).
In addition, there are common
neurobiological bases among humans and other
primates in the control of facial
expression. A recent study of projections
from the cortex to the facial nerve nucleus in
rhesus macaques found a pattern similar to that
described by Rinn (1984). Bilateral cortical
projections to facial nuclei control frontalis
and orbicularis oculi muscles, and contralateral
projections to the opposite facial nucleus,
control the muscles aroundthe mouth, allowing
hemispheric differences in expressiveness to
influence the lower face in particular
(Morecraft et al., 2001). Researchers have begun
to demonstrate asymmetry in facial expressions
of monkeys, indicating that these underlying
mechanisms of control also produce similar
effects in non-human primates. Hook-Costigan and
Rogers (1998) found that positive social calls
and expressions of marmosets were lateralized to
the right, while negative social expressions
(fear) were lateralized to the left. Hauser and
Akre (2001) also found that expressions were
seen earlier on the left side of the face in
rhesus macaques, although they found no
different between expressions interpreted as
socially positive or negative, expanding on the
original finding by Hauser (1996) that rhesus
expressions were leftsided. Although at least
some degree of neurobiological and physical
homology of expression seems likely, there is
also the problem of differential function. Can
human smiles really be homologous to the SBT
display when human smiles signal joy and
nonhuman primate smiles signal appeasement or
fear? From the perspective of human facial
expression, the roles of the smile continue to
expand with new research, and the equation of
human smiles withhappiness has been called into
question (Ekman, 1985; Fridlund, 1994). Nonhuman
primate bared teeth displays (as in Fig. 6) may
be similar in meaning and function to human
smiles, depending on the socioecological
context. Human anger expressions and ape
anger/fear expressions may also be homologous
(Chevalier-Skolnikoff, 1973). Embarrassment has
been proposed as a homologue of primate
appeasement displays, because it shares
characteristics such as withdrawal, minimizing
appearance, and smile with downward glance
(Keltner and Buswell, 1997). Homology has also
been proposed for the yawn, which shows evidence
of being a social signal of transition between
activity states both in humans and in nonhuman
primates (Deputte, 1994; Provine, 1997).
Homology may also apply to aspects of hiding or
minimizing expression. There are several
examples of apes preventing conspecifics from
seeing their expression by covering the face
with a hand (Tomasello and Call, 1997), and one
report of a chimp that was able to control a
grimacing mouth by pressing down on his lips
with his hand (Mitchell, 1999).Humans also move
their hands to the face to hide expressions,
possibly because such expressions would be
detrimental to their interests if openly
recognized (Keltner and Buswell, 1997) for
embarrassment; see Provine (1997) for
yawning.
Humans have the additional ability of hiding
their expressions with the actions of other
facial muscles, especially around the mouth
where the downward pull of the depressor anguli
oris muscle can somewhat conceal the rise of the
lip corners due to the action of zygomaticus
major (Ekman, 1985). Spontaneous expressions may
have elements of concealment associated with
them, such as "twisting" the smile to avoid
appearing too pleased in front of others
(Friedman and Miller-Herringer, 1991). In the
same study, the authors noted that hand contact
increased with increased smiling. It could be
that the action of other facial muscles in some
cases was inadequate to the task of concealing
the increasingly obvious smile signal.
Consideration of nonhuman primate facial
expression, of course, is necessarily be
specific to each individual species. Divergent
facial signaling systems, as well as some
homology, are to be expected. For the
relationship between overall amount of
expression and the structure of the facial nerve
nucleus, Peburn et al. (2000) found variation
betweenspecies, with the relatively more
expressive macaques (Macaca fascicularis)
showing significantly larger and better defined
facial subnuclei than the relatively less
expressive patas monkeys (Erythrocebus patas).
Aotus, the only nocturnal anthropoid, has
virtually no facial expression, and its facial
musculature is also relatively less
differentiated (Chevalier- Skolnikoff, 1973;
Huber, 1931).
Likewise, many features of human facial
expression, although universal, are specific to
our species. The relative hairlessness of the
human face, compared to the majority of nonhuman
primates, suggests that the combination of
exposed skin and retainedhair may have some
signaling value. Brows are an important
component of human greeting andsurprise
displays, as well as some smiles. Upturned inner
brows also signal sadness or grief
(Eibl-Eibesfeldt, 1989; Ekman, 1979). Results of
an intriguingstudy in which cross-species
perception offacial expression was tested, the
brows, a highlyvisible signal on the hairless
human face, are notused by macaques seeking to
identify sad humanfacial expressions. They rely
instead on other, morephylogenetically conserved
traits, such as cheekmovement (Kanazawa, 1998).
Retention of facialhair in adult male humans may
also play a role inaccentuating or concealing
expression. Unfortunately,there has been no
research on male facialhair as it relates to
facial expression.Functions of facial
expressions in nonhumanprimatesLike humans, many
nonhuman primate speciespay close attention to
the faces of other group members.
The complexity of face perception and
facial expression among the great apes, for
example, is just beginning to be demonstrated.
Chimpanzees can use facial features to recognize
both kin andunfamiliar conspecifics, and to
categorize facial expressionsof other
chimpanzees (Parr et al., 1998,2000; Parr and
deWaal, 1999). Chimpanzees canfollow the gaze of
another individual by paying attentionto its
face (Povinelli and Eddy, 1996).
Gorillas,chimpanzees, and bonobos have all been
reportedto monitor the gaze of others, in ways
thatsuggest they may be able to anticipate the
impact oftheir facial expressions on others'
behavior (Mitchell,1999). Clearly, facial
expressions are importantsignals in the social
lives of most nonhuman primates,just as they are
for humans.By monitoring facial expressions, the
intentions ofothers can be inferred. Because of
their relativelystable existence, social groups
provide an environmentin which low-cost,
redundant signals can helpprimates to keep track
of the other individual, possiblysimilar to that
which Chadwick-Jones (1998)described for
baboons. Cheater males may fail togive
continuous signals, and so must be monitored.The
failure to adhere to social scripts,
includingfacial expression patterns, draws
attention to uncooperative individuals
(Mitchell, 1999). Groups of nonhuman primates
may also utilize redundant,"cheap" vocal signals
in order to coordinate theiractivities (Silk et
al., 2000). Haslam (1997) provideda list of
social grammars for primate
interaction,including communal sharing,
authority ranking,equality matching, and market
pricing.These arebehavioral contexts of the type
that could correspondto functional variation in
primate facial expression.As in humans,
considering facial expressionsas adaptations
would require specification ofrelevant
phenotypes, ecological contexts, and positiveand
negative fitness consequences.
CONCLUSIONS : Current functional
approaches to facial expression are largely
framed in terms of the proximate functions of
emotions associated with that expression(Keltner
and Gross, 1999; Keltner and Haidt,1999; Yik and
Russell, 1999). Fridlund (1994) hasargued from a
critical psychological perspective forthe
consideration of all facial behavior in a
behavioralecological or evolutionary
framework.
Evolutionary approaches, however, are
necessarily basedon the study of facial
expressions as biological adaptations,and much
of the recent work on facial expression has been
conducted outside this perspective.
Nevertheless, results from this type
offunctional study of facial expression provide
a basison which to base evolutionary hypotheses
of facial behavior. By detailing the phenotypic
variation infacial expression, clearly defining
the ecological contextsof facial expression, and
describing some of thepositive fitness
consequences of these behaviors, wehave outlined
an evolutionary approach to the study of human
facial expressions as adaptations. By proposing
testable hypotheses about the nature of facial
expression, we can also provide a firm
biological basis to other anthropological
studies of communication. The unfortunate,
and probably unintended,view of nonverbal
expression as representing an ancestral-primate
primitive ability, whilelanguage is uniquely
specialized in humans, canalso be challenged
from this perspective (Eibl-Eibesfeldt, 1989).
Instead of just assuming that nonverbal
expression has much in common with primate
relatives, but is also culturally patterned, w
emay be in a position to specify more clearly
theadaptive role of facial expression in human
social interaction.Human social intelligence is
obviously a major contributor to human brain
evolution and intellectualabilities. Our most
specialized and adaptive system of social
signaling is human language (Pinker, 1994).
Remarkable in its complexity andalso because of
its seeming discontinuity with nonhuman primate
vocalization and communication, human language
has clear adaptive consequences for human
evolution (Burling, 1993; Pinker, 1994).There is
no doubt that language has been a driving force
in the evolution of human behavior, and the
social context is dominated by language
(Dunbar,1996). Yet there is more to social
intelligence than language. Deficits in other
social skills, including nonverbal skills, make
it very clear that language alone is not
sufficient for successful social interaction,and
the positive consequences of these skills are
only now being described. This argues for
increased attention to the evolution of
nonverbal signaling systems, including facial
expression, from theperspective of physical
anthropology.
