Symmetry Is Related to Sexual Dimorphism in Faces:
Data Across Culture and Species
Anthony C. Little
1
*, Benedict C. Jones
2
, Corri Waitt
3
, Bernard P. Tiddeman
4
, David R. Feinberg
5
, David I.
Perrett
6
, Coren L. Apicella
7
, Frank W. Marlowe
8
1 School of Psychology, University of Stirling, Stirling, United Kingdom, 2 School of Psychology, University of Aberdeen, Aberdeen, United Kingdom, 3 Department of
Zoology, University of Oxford, Oxford, United Kingdom, 4 School of Computer Science, University of St Andrews, St Andrews, United Kingdom, 5 Department of
Psychology, McMaster University, Ontario, Canada, 6 School of Psychology, University of St Andrews, St Andrews, United Kingdom, 7 Department of Anthropology,
Harvard University, Cambridge, Massachusetts, United States of America, 8 Department of Anthropology, Florida State University, Tallahassee, Florida, United States of
America
Abstract
Background: Many animals both display and assess multiple signals. Two prominently studied traits are symmetry and
sexual dimorphism, which, for many animals, are proposed cues to heritable fitness benefits. These traits are associated with
other potential benefits, such as fertility. In humans, the face has been extensively studied in terms of attractiveness. Faces
have the potential to be advertisements of mate quality and both symmetry and sexual dimorphism have been linked to the
attractiveness of human face shape.
Methodology/Principal Findings: Here we show that measurements of symmetry and sexual dimorphism from faces are
related in humans, both in Europeans and African hunter-gatherers, and in a non-human primate. Using human judges,
symmetry measurements were also related to perceived sexual dimorphism. In all samples, symmetric males had more
masculine facial proportions and symmetric females had more feminine facial proportions.
Conclusions/Significance: Our findings support the claim that sexual dimorphism and symmetry in faces are signals
advertising quality by providing evidence that there must be a biological mechanism linking the two traits during
development. Such data also suggests that the signalling properties of faces are universal across human populations and
are potentially phylogenetically old in primates.
Citation: Little AC, Jones BC, Waitt C, Tiddeman BP, Feinberg DR, et al. (2008) Symmetry Is Related to Sexual Dimorphism in Faces: Data Across Culture and
Species. PLoS ONE 3(5): e2106. doi:10.1371/journal.pone.0002106
Editor: Thomas Reimchen, University of Victoria, Canada
Received July 9, 2007; Accepted March 7, 2008; Published May 7, 2008
Copyright:
2008 Little et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits
unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: Anthony Little is supported by a Royal Society University Research Fellowship. Frank Marlowe is sponsored by the National Science Foundation grant #
0650574. David Perrett is supported by Unilever research. No funders had any role in the conduct or any other aspect of this paper.
Competing Interests: The authors have declared that no competing interests exist.
* E-mail: anthony.little@stir.ac.uk
Introduction
Increasingly attention is being paid to the complexity of animal
signalling [1]. Many animals display multiple traits and assess
multiple signals. Multiple traits may be signals of the same factor,
and so serve to enhance the accuracy with which receivers assess a
single factor, or else signal different facets of an individual’s quality
[2]. In terms of sexual selection, signalling traits can be divided by
their role in intrasexual (same-sex competition) and intersexual
(choices of the opposite-sex) selection. While faces are likely to play
a role in same-sex competition [3], it is the later form of sexual
selection that has been most prominently applied to research on
human facial attractiveness.
Darwin [4] laid out the first notions of how evolution of traits by
preference could occur. Self-reinforcing, or ‘‘runaway’’, selection
[5] may explain certain traits. After a preference for any particular
trait has arisen, for example, a preference for long tails in a bird
species, females begin to reproduce with males in possession of
long-tails to produce offspring with both genes for long tails (in
males) and genes for a preference for long tails (in females). A
feedback loop between genes for traits and preferences produce
stronger preferences and ever more elaborate expression of traits.
The initial preference could come from a sensory disposition
evolved for another purpose [6] and hence arbitrary. The idea that
male or female morphology may be attractive because it exploits
an already existing preference in the opposite-sex has been called
the perceptual or sensory bias view [7].
In contrast to such views, indicator mechanisms of sexual
selection propose that certain traits are preferred because they are
associated with either phenotypic or genotypic quality [8] and
therefore act as cues and hence can be signals of quality. A key
concept in indicator mechanisms is the notion of handicaps.
Individuals may find mates who carry a costly handicap more
attractive because the fact they have survived with the handicap is
an indicator of their genetic quality [9]. Many traits also require
energy to produce and so individuals must be in good condition to
afford their production. Handicaps can then be ‘honest’–low
quality individuals cannot ‘fake’ such traits. Individuals who
choose partners in possession of such traits will produce more
offspring than those who do not.
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An important question is whether particular traits are driven by
indicator mechanisms or are driven by arbitrary preferences.
Researchers have suggested that different signals of the same
quality should inter-correlate [10,11], which would support
indicator mechanisms in their evolution. For example, in humans,
the judged attractiveness of female bodies correlates with facial
attractiveness [11] and the pitch of female voices also positively
predicts facial attractiveness [12]. Both studies suggest that the
three traits measured are in part signalling one aspect of quality.
Such a relationship should come about because the underlying
quality advertised by one trait will also be reflected in other traits.
If traits advertise discrete aspects of quality, then there is no apriori
reason to expect such traits to co-vary. Theories suggesting that
traits are being driven by perceptual bias or via arbitrary runaway
selection also do not predict co-variation.
Two important traits thought to relate to mate-quality in many
animals are symmetry and sexual dimorphism [13,14]. Fluctuating
asymmetry (FA) [15] is thought to reflect an individual’s ability to
maintain the stable development of their morphology under the
prevailing environmental conditions. Fluctuating asymmetry is a
useful measure as it subsumes a large amount of individual
variation in development, reflecting differences in genetic (e.g.,
inbreeding, mutation, and homozygosity) and environmental (e.g.,
nutrient intake, parasite load) factors [16]. While the issue is
controversial [17], many studies do show links between symmetry
and quality including factors such as growth rate, fecundity,
fertility and survivability [16,18,19] and one study has shown that
symmetry in both men and women is negatively related to self-
reported health problems [20]. Potentially, any link between
symmetry and quality, no matter how weak, may be sufficient to
create a selection pressure to choose symmetric mates. Symmetry
in human faces has then been suggested to be a cue to heritable
fitness benefits [21,22] and studies of real [23,24] and manipulated
faces [22,25] show that symmetry is found attractive. Facial
symmetry is found attractive in different human cultures [26] and
in monkey species [27].
In some species sexually dimorphic traits advertise genetic
quality [14]. Larger jawbones, more prominent cheekbones, and
thinner cheeks are all sexually dimorphic features in human faces
characteristic of males [28,29]. Such masculine features are
associated with higher testosterone in males [30] while feminine
features are associated with higher oestrogen in females [31].
Secondary sexual characteristics may be linked to parasite
resistance because the sex hormones which influence their growth,
particularly testosterone, lower immuno-competence [32]. Larger
secondary sexual characteristics should be related to a healthier
immune system because only healthy organisms can afford the
high sex hormone handicap on the immune system that is
necessary to produce them [33]. There is evidence in humans that
testosterone acts as an immunosuppressant [34] but the data for
women is less clear (see discussion). Testosterone may have a
greater impact on immune function than oestrogen making
sexually dimorphic features more costly for males.
Perceived masculinity in human faces is positively correlated
with males’ long-term health as assessed from medical records [35]
and from self-reports [20]. Sexual dimorphism may also be linked
to other mechanisms of quality advertising through links with
testosterone, which influences behaviour [36]. In women feminin-
ity may also be linked to fertility through an association with
oestrogen [31]. Sexual dimorphism in faces, another proposed
marker of genetic quality [21,29,37], also influences preferences.
Males prefer feminised female faces and females show increased
preferences for masculinity in contexts consistent with masculinity
signalling some aspect of quality [38,39].
If symmetry and masculinity honestly indicate the quality of
individuals, high quality individuals should develop large sexual
ornaments which have little asymmetry. There is evidence for this
within and across bird species where larger ornaments, such as
tails, tend to be more symmetrical than smaller ornaments [13].
Associations between symmetry and trait size are more consistent
with indicator models than an arbitrary process [8,13]. If quality
was unrelated to size and symmetry we would expect the cost of
ornamentation to create developmental stress for their owners
leading to increased asymmetry in large ornaments. However, if
only high quality individuals are capable of bearing the handicap
of growing large traits or symmetric traits we would expect size
and symmetry of traits to correlate.
If symmetry and sexual dimorphism in faces indicate quality
then a positive correlation between symmetry and sexual
dimorphism would be predicted. Evidence for associations
between symmetry and sexual dimorphism in men and women
is equivocal, however [23,24,40,41], and as of yet only city-based
student samples have been examined.
Here we examined the relationship between measured facial
symmetry and facial sexual dimorphism in human population
samples from Europe and from an environment likely to reflect
humans living under more evolutionary relevant conditions (the
Hadza of Tanzania, Africa) as well as in a non-human primate
(rhesus macaques, Macaca mulatta). We measured facial symmetry
and sexual dimorphism from landmark points and tested for
relationships between symmetry and sexually dimorphic propor-
tions. We also tested if composites of symmetrical faces within each
sample were perceived as being more sex-typical than composites
of asymmetric faces.
Materials and Methods
Photographs
For the European images, male (177 individuals) and female (318
individuals) participants had their photograph taken in the
laboratory with a digital camera under standardised lighting
conditions. Participants were asked to pose with a neutral expression
and to look directly into the camera to produce front on facial
photographs. Participants were asked not to smile and to relax their
face during photographs. Neutral expressions (as posed by our
participants) can be seen in the average faces presented later. All
individuals were less than 30 years old (ranging from 17–29,
mean = 20.6, SD = 2.2). Participants were UK based university
students who volunteered to take part in psychology studies and were
primarily UK residents. The photographs were taken at the
universities of Liverpool, Stirling, and St Andrews. Written consent
was obtained for all participants and the collection of photographs
was approved by relevant ethics committees at each institution.
The macaque and Hadza images could not be collected under
laboratory conditions. For the macaque images, a digital video
camera was used to capture images of adult males (105 individuals)
and females (111 individuals) from the free-ranging population of
rhesus macaques on Cayo Santiago, Puerto Rico. Only full-face
images with neutral expressions were used, taken from video
footage. All macaques had identifying tattoos, which were noted
during image acquisition by CW, ensuring that all individuals
included were unique. Images were collected from Cayo Santiago
field station, the Primate Ecology Section of the National Institutes
of Health Laboratory of Perinatal Physiology, which abides by US
laws and practices in the ethical treatment of animals.
For the Hadza images, male (67 individuals) and female (69
individuals) participants had their photograph taken with a digital
camera under variable outside lighting conditions. Participants
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were asked to pose with a neutral expression and to look directly
into the camera. Head tilt and variation was evident for Hadza
images and so images were selected by ACL on the basis of having
a young adult appearance, a neutral expression, and they were
looking directly the camera. Images were taken by FWM and the
full set represented the majority of Hadza. Perceived age was used
to select Hadza images and examining the composite images
below show the average perceived ages. Verbal consent was
obtained for all participants and the collection of photographs was
approved by Harvard’s ethics internal review board. Written
consent was not obtained due to constraints in the field and posing
for the photographs implies implicit consent.
Measurements
We estimated horizontal asymmetry from x-y co-ordinates of 6
bilateral points following techniques used in previous studies
[23,24,37] (see Figure 1). Briefly, symmetry was calculated by
taking left and right deviation from the midline, calculated from
inter-pupillary distance, for points and then summing the absolute
value of individual scores. These symmetry measurements have
been found to correlate with perceived measures of symmetry [24].
While pictures were initially screened for head tilt there was still
the potential for outliers in facial asymmetry. For the full set,
including all image types, mean asymmetry ranged from 5.8 to
187.7 with a mean of 50.0 and a standard deviation of 29.4. This
suggested extreme values beyond two standard deviations (109)
and so we adopted a conservative criterion of 120 to remove
potential outliers. Any images with asymmetry scores higher than
120 were then excluded from the analysis for all sets. This
removed 27 images from the original set of 874.
Sexual dimorphism measures were also taken from points
marked on facial features (Figure 1). The identification of these
features has been found to be reliable in previous studies [23,37].
Following earlier studies, faces were standardised on interpupillary
distance to eliminate variation in head distance from the camera.
This is of particular importance for the Hadza and macaque
images taken under non-standard conditions at varying camera
distances. Colour differences between the images are irrelevant for
measurements as they involve only shape information.
In total, four sexual dimorphism measurements were taken.
These were Cheekbone Prominence (ChP, D3/D6), Jaw Height/
Lower Face Height (JH/LFH, D9/D8), Lower Face Height/Face
Height (LFH/FH, D7/D8), and Face Width/Lower Face Height
(FW/LFH, D3/D8). These were found to be sexually dimorphic
in the European sample here (see below) and in previous studies
[24]. JH/LFH is a new measure here.
Descriptives and distributions of scores
Descriptives for each variable split by image type and sex of
image can be seen in Table S1. Kolmogorov-Smirnoff tests were
used to test for normality of distribution (presented in Table S1).
Significant deviation from normality was seen notably for
asymmetry in the European sample in both men and women.
This was the result of a skew towards low asymmetry for these
measurements from these image sets.
Fluctuating asymmetry and directional asymmetry
The six measures of asymmetry (D1 to D6) may display
fluctuating asymmetry, (FA, right minus left approx 0) or
directional asymmetry (DA, right minus left deviates from 0).
We randomly selected 50 images from each grouping (male/
female6macaque/ European/Hadza) so that each image set was
equally represented in the following calculations. We calculated
scores for right-left for each trait and conducted 1-sample t-tests
against 0 to test for deviations. This revealed directional
asymmetry for 4 traits. If traits exhibit DA then some individual
variation may be due to heritable variation rather than being a
measure of developmental stability [42]. We must then exercise
some caution in concluding that such measures reflect only
developmental stability. While the differences are significant, we
do note that the proportions do not indicate uniformity of
direction (i.e., it is not true that, for example, the distance from the
inner eye to the midline is always greater on the right hand side of the
face) . We note also the large sample sizes here allow us to see small
effects and that there is a positive correlation between a composite
score of FA and a composite score of DA traits (r = .174, p =.003)
indicating the measures tap the same underlying factor. Most
importantly, while 4 of the 6 traits demonstrate DA this does not
mean that a significant proportion of the measure is DA. Our
measure represents FA+DA. For each face we computed a second
measure taking the difference from the average difference from the
mean for each trait. For this score the mean is exactly 0 and
represents an estimation of FA only, controlling for average genetic
or other effects that cause the trait to be directional in nature. The
correlation between our origi-
nal measure and this second number for our sample is very high
(r = .96, p,.001, r
2
= .92) indicating that DA likely accounts for only
8% while FA accounts for 92% of the variance in our original
measures. This suggests our measure largely reflects FA and not DA.
See Table S2 for descriptive statistics of asymmetry.
Sexual dimorphism in measures
Multivariate ANOVA’s were carried out with sex of face as the
fixed factor and masculinity measures as the dependent variables.
For Europeans this revealed significant sexual dimorphism for all
traits, with females scoring higher for FW/LFH (F
1,493
,=57.2,
p,.001) and ChP (F
1,493
,=82.8, p,.001) and males scoring higher
for JH/LFH (F
1,493
,=53.0, p,.001) and LFH/FH (F
1,493
,=45.6,
p,.001). For Hadza this revealed significant sexual dimorphism for
FW/LFH (F
1,134
, = 26.7, p,.001) and ChP (F
1,134
,=8.1, p = .005),
with females scoring higher for both these traits but no signifficant
differences for JH/LFH (F
1,134
,=0.1, p = .75) and LFH/FH
(F
1,134
,=0.4, p = .53). For macaques this revealed significant or
Figure 1. Measurements for symmetry and sexual dimorphism.
Symmetry was calculated by taking left and right deviation from the
midline, calculated from inter-pupillary distance, for points D1-D6 and
then summing the absolute value of individual scores. Sexual
dimorphism was measured by measuring distance between specific
points and calculating four ratios based on these distances: Cheekbone
Prominence (ChP, D3/D6), Jaw Height/Lower Face Height (JH/LFH, D9/
D8), Lower Face Height/Face Height (LFH/FH, D8/D7), and Face Width/
Lower Face Height (FW/LFH, D3/D8). All images were normalised on
inter-pupillary distance.
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near significant sexual dimorphism for all traits, with females scoring
higher for ChP (F
1,214
,=4.7,p = .031) and males scoring higher for
JH/LFH (F
1,214
,=9.3,p =.003),LFH/FH(F
1,214
,=141.5,p,.001)
and FW/LFH (F
1,214
,=3.5, p =.061).
Correlations between measures of masculinity and with
symmetry
Tables S3, S4, and S5 show the correlations between all of the
variables for each image set and for male and female images. The
correlations with asymmetry are equivalent to the results of the
regression analysis as only a single variable persists in each analysis.
Making composite images
The 15 highest and lowest asymmetry scores for males and
females were selected to make up the composites. For each set of 15
face images a single composite face was produced. The composite
faces were created using specially designed software. Key locations
(174 points) were manually marked around the main features and
the outline of each face. The average location of each point in the 15
faces for each composite was then calculated. The features of the
individual faces were then morphed to the relevant average shape
before superimposing the images to produce a photographic quality
result. For more information on this technique see [43,44].
Composite images can be seen in Figure 1.
As the Hadza and the macaque images differed in lighting
conditions we blended the shape and colour of the symmetric and
asymmetric version together for each pair and then applied only
the resultant colour to each original pair. This meant all images
were standardised within pairs, so that both images possessed the
same basic colouration. Images were also cropped to display only
facial information.
An additional set of composite pairs were created for control
purposes. These were made using the same methods as above but
consisted of 15 randomly selected images from the appropriate
groups. While random these images were labelled in the same
manner (symmetric/asymmetric).
Rating the composite images
Participants. 50 individuals (27 female, mean age 28.8,
SD = 6.7) judged the symmetric/asymmetric composites. 37
individuals judged the random composites (23 female, mean age
28.3, SD = 10.7). All individuals were volunteers responding to link
on an electronic poster system and were UK based university
students.
Procedure. Participants were administered a short
questionnaire assessing age and sex before completing the face
tests. The 6 pairs of symmetric and asymmetric faces of each sex
were presented in separate blocks. Male faces were rated first,
followed by female faces. Faces appeared on the screen side by
side. Both order and side of presentation were randomised.
Participants were asked to choose the face of the pair that they
found most typical for that sex (i.e., for male faces: ‘‘which face
appears most typical of males’’). This action initiated the next face
trial. A second set of participants completed the same trials but
using the random composites.
Results
Measurements: composite measures of sexual
dimorphism
In order for comparison amongst face type scores were
standardised separately by face-type so that the mean for each
group was 0 with a standard deviation of 1. An overall asymmetry
score (sum of the absolute vales of deviation from midline for D1-
D6) and an overall masculinity score ([JH/LFH+LFH/FH]-
[ChP+ FW/LFH]) were calculated.
A univariate ANCOVA was conducted with asymmetry as the
dependent variable, face-type (European/Hadza/Macaque) as a
factor, and average masculinity as covariate. For female faces this
revealed masculinity was not significantly related to asymmetry
(F
1,452
= 2.10, p = .148). Other effects and interactions were not
significant (F
2,452
,2.44, p..088). For male faces this revealed
masculinity was significantly related to asymmetry (F
1,343
= 12.09,
p,.001). Other effects and interactions were not significant
(F
2,343
,1.23, p..295). Pearson product moment correlations
between asymmetry and masculinity revealed that there was no
significant correlation for female faces (r = 20.48, p = .285) and a
significant negative correlation for males faces (r = 2203, p,.001).
As a secondary analysis we conducted a discriminant analysis
using the four sexually dimorphic measures to discriminate sex of
face separately for each face-type. Groups differed based on
classification: European (Wilks’ Lambda = .74, X
2
= 148.98,
DF = 4, p,.001), Hadza (Wilks’ Lambda = .78, X
2
=33.11,
DF = 4, p,.001), and macaque (Wilks’ Lambda = .96, X
2
=8.25,
DF = 4, p = .083). Classification was correct/incorrect: female 346/
152, male 238/111. A univariate ANOVA was conducted with
asymmetry as the dependent variable, and face-type (European/
Hadza/Macaque), sex (male/female), and classification (male/
female) as factors. This revealed a significant interaction between
sex and classification (F
1,835
=4.07, p = .044). The interaction
reflected that faces that were misclassified according to facial
measures demonstrated greater asymmetry than faces that were
classified as sex typical (see Figure 2). A theoretically unrelated
significant interaction between face-type and classification was also
found (F
1,835
=4.37, p = .012). Other effects and interactions were
not significant (F
1/2,343
,1.22, p..296).
Measurements: regression of sexually dimorphic traits by
sex and face-type
Overall asymmetry score was predicted using the four individual
measures of sexual dimorphism (see Methods) entered into a
Figure 2. Asymmetry (+/2 1SE of mean) of faces classified as
male or female in the discriminant analysis by sex of face.A
significant interaction was found between sex of face and classification
(F
1,835
= 4.07 , p = .044) indicating that those correctly classified to their
own sex were more symmetric than those misclassified to the opposite-
sex.
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backwards linear regression analysis (p = .1 criteria, only the final
model is reported here). Measures of sexual dimorphism were
treated separately as correlations between these traits were
generally low. For full interrelationships between measures of
symmetry and sexual dimorphism see Tables S3, S4, and S5.
For European faces, the model was close to significant for
females (F
1,316 =
3.1, p = .080, R
2
= .01) where the masculine trait
LFH/FH was positively related to asymmetry (b= .10, p = .080).
The model for males was significant (F
1,175 =
6.6, p = .011,
R
2
= .04) where the masculine trait JH/LFH was negatively
related to asymmetry (b= 2.19, p = .011).
For Hadza faces, the model was not significant for females with
no significant predictors (all p..23) but was significant for males
(F
1,65 =
7.1, p = .010, R
2
= .10), where the masculine trait JH/LFH
was negatively related to asymmetry (b= 2.31, p = .010).
For macaque faces, the model revealed a significant model for
females (F
1,109 =
4.6, p = .035, R
2
= .04), where the masculine trait
JH/LFH was positively related to asymmetry (b= .20, p = .035).
The model for males was also significant (F
1,103 =
4.0, p = .047,
R
2
= .04), where the masculine trait LFH/FH was negatively
related to asymmetry (b= 2.19, p = .047).
The results of this analysis are robust to corrections for multiple
tests (see Text S1, Table S6).
Perception of composites
Measured sexual dimorphism may not capture all aspects of this
trait to which humans are visually sensitive. To examine
perception, composite images of individuals with high and low
facial asymmetry were created for males and females of each
population (see Methods, Figure 3). These image pairs were shown
to European human participants, who were asked out of the pair
which was more typical of their sex in appearance. Chi square tests
were conducted on the proportions showing that, for females,
symmetric Hadza (x
2
= 5.1, p = .021) and Europeans (x
2
= 25.9,
p,.001) were selected as more typically female than asymmetric
Hadza and Europeans. Proportions were not significantly different
for female symmetric and asymmetric macaques (x
2
= 0.7, p = .40).
For males, symmetric Hadza (x
2
= 2.9, p = .088, p = .044 one-
tailed as predicted from measurement data), macaques (x
2
= 3.9,
p = .048), and Europeans (x
2
= 8.0, p = .005) were selected as more
typically male than asymmetric Hadza, macaques, and Europeans.
Proportions can be seen in Figure 4. A binomial test revealed that
the proportion of symmetric images being chosen as most sexually
dimorphic significantly differed from chance (chosen = 6/6,
chance 3/6, p = .031).
Comparing the overall scores to chance (50%) using one-sample
t-tests revealed that the choice of symmetric/asymmetric compos-
ites differed from chance (mean = 67%, SD = 17%, t
49
= 7.01,
p,.001) while the random composites did not (mean = 47%,
SD = 17%, t
36
= 7.01, p = .337). An independent-samples t-test
revealed a significant difference in choice between symmetric/
asymmetric and random composites (t
85
= 5.36, p,.001). Thus the
overall pattern for the composites was that symmetric images were
seen as more sexually dimorphic in humans and male macaques
using both chance and a control set of images as criterion.
Discussion
Our results indicate that symmetry and sexually dimorphic traits
are related in male and female faces in humans, in a modern
western society and in a different society living under conditions
better approximating human evolutionary history, and across
species, both in humans and a non-human primate. We found
symmetry was related to sexual dimorphism using physical
measurements of large numbers of faces and perceptual tests
based on the perceived sexual dimorphism of faces that were most
and least symmetric in our samples. We note that only European
participants provided the ratings of the composites and it is likely
Figure 3. High and low symmetry composite faces for
macaques, Hadza, and Europeans. All images are normalised on
inter-pupillary distance to control relative image size, have been made
perfectly symmetric, and each high/low pair possesses the average
colour information of both. Perceptual differences are then dependent
on shape differences between high and low symmetry faces that are
independent of symmetry.
doi:10.1371/journal.pone.0002106.g003
Figure 4. Proportion of individuals choosing high and low
symmetry composite faces for macaques, Hadza, and Europe-
ans as most sex-typical (i.e. masculine for males, feminine for
females).
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difficult for them with limited experience to judge masculinity in
Hadza and macaque faces. In fact this raises an interesting point.
The generally consistent judgement that symmetric individuals
appeared more sexually dimorphic across all face types from
European judges that there is some commonality in features that
cross culture and species.
We note that the measurements may not necessarily capture
sexual dimorphism fully (as suggested by the discriminant analysis)
but that together the patterns of the measurement and perceptual
data supports the notion that sexual dimorphism and symmetry in
faces are linked. We also note that some caution must be taken in
interpretation as our symmetry measurements do not all fully fulfil
the criteria for fluctuating asymmetry, though appear to mainly
capture FA and not DA (see Methods). The DA in our measures
might reflect expressive habits, for example, natural smiles are
asymmetric reflecting hemispheric specialisation in the control of
emotion [45]. We also note that the different types of analysis
reveal some differences in sex effects as sexual dimorphism was not
found to be related to symmetry using an additive measure
whereas a relationship emerged in the discriminant analysis. The
overall pattern, however, is that symmetry was related to some
aspect of dimorphism either via one aspect of measurement:
overall additive or discriminative measurements, individual trait
measures, or perceptual measures.
If sexual dimorphism and symmetry in faces advertise quality in
both males and females then only high quality males can grow
symmetric and masculine and high quality females can grow
symmetric and feminine. Similar arguments have been put
forward to explain co-variation between trait size and symmetry
in birds [13]. This relationship then suggests that notions of
symmetry and sexual dimorphism signalling a single aspect of
quality are true. We also note, however, that the relationship is not
absolute, leaving the potential that both may also signal other
separable qualities. Symmetry and sexual dimorphism may then
be seen as complementary signals of the same quality, but may also
signal other qualities independently. Previous studies have shown
negative associations between symmetry and trait size in the
secondary sexual traits of a variety of taxa, including birds and
primates [3,13]. The results here demonstrate that faces are
involved in selection with no obvious association with weaponry
involved in intra-sexual selection, as shown in previous studies of
primate tooth dimorphism. Bare skin on faces in primate species is
common [46], further highlighting the potential role for sexual
selection acting on faces across the primate lineage.
Sexual dimorphism is facilitated by sex hormones [47].
Symmetry is linked to developmental stability [16]. Symmetry
and sexual dimorphism may be linked by an underlying biological
factor. For example, both may reflect gene quality. If high quality
genes are those that code, potentially, for efficient immune
systems, high metabolic efficiency, or even behavioural traits that
secure resources for an organism during development, then such
genes may also allow an organism to grow both symmetric and
sexually dimorphic. By measuring how well an organism can cope
with genomic stress and environmental perturbations, symmetry
may be an honest signal of gene-quality given that studies show
that such stressors during development increase asymmetry [48].
The link between sexual dimorphism and good-genes advertise-
ment has produced many more theories. Honest signalling in this
case might arise through an immuno-competence handicap
mechanism [49], whereby sex hormones represent a behavioural
or immunological handicap to the organism. Other mechanisms
may also create honesty in hormone mediated traits, for example
via cortisol levels [50]. Theoretically, honesty can also arise, when
high-quality individuals achieve greater benefit from an allocation
to a trait than do low-quality individuals even when the costs of the
trait are equivalent [51]. Mate choice based on symmetry and
sexual dimorphism may then provide indirect benefits, acquiring
good-genes from partners that benefit offspring, or direct benefits,
acquiring factors other than good-genes from partners that benefit
the choosing individual, such as resources. Of course there are
other potential benefits of sexual dimorphism and symmetry, for
example fertility [19,31]. Ultimately it may be unnecessary to
consider the relative weights of indirect and direct benefits as they
are difficult to tease apart. For example, males with good-genes for
immunity may also be most able to provide food or defend a large,
high quality territory; thus selection for good resources/behaviour
may reflect selection for good-genes.
The current study shows that symmetry and sexual dimorphism
are related in both male and female faces across cultures and
species. Examining the regression models suggests that the
relationship between symmetry and sexual dimorphism is stronger
for males than for females for both the European and Hadza
samples; Hadza males also retain symmetry with age more than
females do [52]. In the additive measures, symmetry was related to
dimorphism only for males, but the discriminant measure was
related in females. Our perceptual test may be biased in examining
sex differences as it is dependent on the number of images in the
sample. For example, we may see the largest effect in females in
the European sample potentially because we had the largest
number of participants in this group, making the composites more
likely to represent the extremes of asymmetry. Following the
regression models then, we do see a more consistent effect in male
faces. The immuno-competence-handicap hypothesis was origi-
nally proposed for males and there is reasonable evidence
testosterone reduces immune function [32]. Weaker relationships
for symmetry and femininity in females may stem from the fact
that the relationship between oestrogen and immuno-competence
appears weaker than between testosterone and immuno-compe-
tence. In humans, higher oestrogen is linked to development of
cancers [53], suggestive of a reduction in immune function,
although animal studies suggest that while suppressing cell-
mediated immunity, oestrogen may enhance humoral immunity
[54]. As feminine facial traits differ less from immature traits than
do male traits [28], they are also potentially less costly to produce.
Taken together these findings suggest that feminine traits may be
less powerful signals of good-genes than masculine traits, although
we note there that here femininity in female faces is correlated
with symmetry, another proposed aspect of quality. Additionally,
our data does not necessarily support the idea that sexual
dimorphism represents a single continuum in faces. We generally
found relatively weak correlations amongst dimorphism measures
(see Tables S3, S4, and S5). Here perhaps we have evidence that
certain face traits may be more involved in sexual selection than
others.
While studies demonstrate that preferences can arise via
experience [55,56], as a by-product of pattern recognition in the
visual system works without either trait being related to quality,
such reasoning does not predict co-variation between traits in
natural populations. It has also been suggested the preference for
symmetry of tails in bird species may in fact be due to
aerodynamics and not developmental stress [17]. While this would
be plausible for a species in which small deviations in symmetry
may have large effects, as is the case for flying, it is difficult to
imagine such small deviations in symmetry would impact on
motor action in faces so much as to appear unattractive. Such
views imply that symmetry and sexual dimorphism preferences are
arbitrary and neither view proposes underlying mechanisms that
would influence the development of both.
Symmetry and Sexual Dimorphism
PLoS ONE | www.plosone.org 6 May 2008 | Volume 3 | Issue 5 | e2106

In conclusion, our finding of sex specific co-variation with
symmetry, femininity for females, masculinity for males, indicates
then that both sexual dimorphism and symmetry likely are signals
advertising quality. We have shown such a relationship in diverse
human cultures and in a monkey species, which suggests that
signalling properties of faces are universal across human
populations and that facial advertisements of quality may have
arisen relatively early in the phylogeny of primates.
Supporting Information
Table S1 Descriptive statistics for measured traits
Found at: doi:10.1371/journal.pone.0002106.s001 (0.07 MB
DOC)
Table S2 Tests for directional asymmetry for the 6 symmetry
traits
Found at: doi:10.1371/journal.pone.0002106.s002 (0.03 MB
DOC)
Text S1 Iterated bonferonni correction of p-values for regression
analysis
Found at: doi:10.1371/journal.pone.0002106.s003 (0.03 MB
DOC)
Table S3 Correlations amongst measures of sexual dimorphism
and Symmetry for macaque sample (female/male).
Found at: doi:10.1371/journal.pone.0002106.s004 (0.03 MB
DOC)
Table S4 Correlations amongst measures of sexual dimorphism
and Symmetry for European sample (female/male).
Found at: doi:10.1371/journal.pone.0002106.s005 (0.03 MB
DOC)
Table S5 Correlations amongst measures of sexual dimorphism
and Symmetry for Hadza sample (female/male).
Found at: doi:10.1371/journal.pone.0002106.s006 (0.03 MB
DOC)
Table S6 Comparison of directional p-values with iterated
Bonferonni corrected significance levels.
Found at: doi:10.1371/journal.pone.0002106.s007 (0.03 MB
DOC)
Acknowledgments
We thank COSTECH for permission to conduct research in Tanzania and
the UK sample and the Hadza for their participation.
Author Contributions
Conceived and designed the experiments: AL. Performed the experiments:
BJ AL CW BT DP. Analyzed the data: AL. Contributed reagents/
materials/analysis tools: CW BT DP CA FM. Wrote the paper: BJ AL CW
DF.
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