Behavioral Ecology Vol. 14 No.

5: 668–678
DOI: 10.1093/beheco/arg043

Major histocompatibility complex genes,

symmetry, and body scent attractiveness in
men and women
Randy Thornhill,a Steven W. Gangestad,b Robert Miller,a Glenn Scheyd,b Julie K. McCollough,a and
Melissa Franklina
Departments of aBiology and bPsychology, The University of New Mexico, Albuquerque,
NM 87131-1091, USA

Downloaded from beheco.oxfordjournals.org at Santa Monica College Library on October 4, 2010

Previous research indicates that the scent of developmental stability (low fluctuating asymmetry, FA) is attractive to women who
are fertile (at high-conception risk points in their menstrual cycles), but not to other women or men. Prior research also indicates
that the scent of dissimilarity in major histocompatibility complex (MHC) genes may play a role in human mate choice. We
studied the scent attractiveness to the opposite sex of t-shirts worn for 2 nights’ sleep. Our results indicate that the two olfactory
systems are independent. We repeated previous results from studies of the scent of symmetry. We repeated previous results from
MHC research in part; men, but not women, showed a preference for t-shirts with the scent of MHC dissimilarity. Women’s scent
ratings of t-shirts were uncorrelated with the wearer’s MHC dissimilarity and allele frequency, but positively correlated with the
wearer’s MHC heterozygosity. Fertile women did not exhibit any MHC trait preferences. Women’s preference for the scent of
men who were heterozygous for MHC alleles may be stronger in women who are at infertile cycle points. Men preferred the scent
of common MHC alleles, which may function to avoid mates with rare alleles that exhibit gestational drive. Men also preferred
the scent of women at fertile cycle points. The scent of facially attractive women, but not men, was preferred. Neither FA nor
facial attractiveness in either sex correlated with MHC dissimilarity to others, MHC heterozygosity, or MHC allelic rarity. Key words:
Homo sapiens, inbreeding, major histocompatibility complex, mate choice, parasites, pheromones, sexual selection. [Behav Ecol
14:668–678 (2003)]

he major histocompatibility complex (MHC) is a highly
T polymorphic gene complex (in humans often referred to
as human leukocyte antigens, HLA genes), that encodes cell-
surface receptors that play a critical role in the initiation of
most immune responses. By binding and presenting peptides
derived from either endogenous or foreign proteins, the
MHC plays a central role in the discrimination of self from
non-self, thereby regulating recognition of infectious diseases.
Host–pathogen coevolution is now generally thought to
explain much of MHC genetic polymorphism because of
MHC’s function in pathogen detection (Apanius et al., 1997;
Hughes and Hughes, 1995; Penn and Potts, 1999).
Increasing evidence indicates that MHC genes influence
body odor and mate choice based on body odor attractiveness.
Most investigations have involved house mice (Mus musculus)
and humans. The mouse studies suggest a preference for
the scent of MHC dissimilarity (Penn, 2002; Penn and
Potts, 1999). In humans, Wedekind et al. (1995) found that
normally ovulating women (e.g., not taking a contraceptive
pill) preferred the scent of men (on t-shirts worn for 2 nights’
sleep) who had MHC genotypes dissimilar to their own. A
second study replicated the MHC-dissimilarity scent prefer-
ence in women not on the pill and, furthermore, found the
same scent preferences in men (Wedekind and Füri, 1997).
Interestingly, participants in these two studies also claimed
that the scents of MHC-dissimilar individuals were reminis-
cent of those of former or current mates. Indeed, Ober et al.
(1997) found that Hutterite married couples tend to be more
MHC dissimilar than expected by chance, an effect that may
Address correspondence to R. Thornhill. E-mail: rthorn@unm.edu.
Received 16 January 2002; revised 25 September 2002; accepted 4
December 2002.
Ó 2003 International Society for Behavioral Ecology
be at least partly mediated by body scent. In contrast, a study
of South American Indians (Hedrick and Black, 1997) and
a study of Japanese couples (Ihara et al., 2000) reported no
evidence for MHC-dissimilar assortative pairing among
married couples (for review, see Penn, 2002).
There are at least four adaptive explanations for MHC-
dissimilarity scent preferences. First, these preferences may
have the evolved function of inbreeding avoidance (see review
of literature on this hypothesis in Penn and Potts, 1999). The
three remaining potential explanations of scent preference
for MHC-dissimilarity are founded upon parasite-mediated
sexual-selection theory. The heterozygosity hypothesis posits
that the preference has evolved because it produces MHC-
heterozygous offspring that have sound immunocompetence
against more parasite types (owing to a wider array of
pathogenic antigens recognized by the immune system, given
that MHC alleles show codominance; Brown, 1997; Wedekind
et al., 1995). Penn et al. (2002) found that heterozygous
house mice are more fit than homozygotes upon encounter-
ing multiple strains of pathogens. The rare-allele hypothesis
claims that the preference functions to obtain rare MHC
alleles for offspring, which give defense against rapidly
evolving parasites that may escape recognition by immune
systems containing common alleles or that may reduce the
risk of autoimmunity possibly associated with common alleles
(Penn and Potts, 1999). The rare-allele hypothesis implies
preference for MHC dissimilarity because, to place the rare
MHC alleles in offspring by mate choice, mate choosers (most
of whom carry relatively common MHC alleles) must choose
the infrequent individuals who are dissimilar because of their
rare MHC genotype. Wedekind and Füri (1997) found no
evidence that particular MHC genotypes were preferred, as
the rare-allele hypothesis implies, but their study examined
responses to only six people’s scents. The diverse-genes
Thornhill et al.
Human scent attractiveness
hypothesis views the function of the preference as obtaining
MHC alleles for offspring that are different from the parents’
own (independent of both production of heterozygous
offspring and offspring with rare alleles) as well as from one
another because pathogens adapted to parents and other
close kin will then be less adapted to offspring (Penn and
Potts, 1999).
A prediction related to the the diverse-genes hypothesis is
that individuals should avoid mating with MHC homozygotes.
Homozygotes have offspring who vary less from each other
and the mate, which increases the risk of a within-family
disease epidemic. The diverse genes hypothesis is supported
by a study of sticklebacks. Females preferred males with many
MHC alleles over males with fewer (Reusch et al., 2001).
According to the first two parasite-mediated sexual selec-
tion hypotheses, the heterozygosity and rare-allele hypothe-
ses, genotypic variation in MHC should be associated with
interindividual phenotypic condition. Specifically, individuals
with MHC heterozygosity or rare MHC alleles are predicted to
be of relatively high phenotypic quality as a result of their
greater resistance to parasites or, in the latter case, reduced
autoimmunity. The outbreeding hypothesis gives no reason to
expect such associations in the case of humans. In our largely
outbred human sample (see below), MHC homozygosity
should not be a reliable marker of being inbred and thus of
low phenotypic quality.
A potentially important phenotypic marker of sound
phenotypic condition and underlying high genetic quality is
low fluctuating asymmetry (FA). FA is nondirectional de-
viation from perfect bilateral symmetry in traits that are, on
average, bilaterally symmetrical. FA reflects ability to deal with
stresses, both genetic and environmental, during ontogeny.
Individual FA, then, is developmental maladaptation or
instability owing to the individual’s inability to achieve perfect
bilateral symmetry given perturbations during traits’ ontogeny
(review in Møller and Swaddle, 1997; Polak, 2003).
Genetic perturbations known to generate FA in traits
include mutations, homozygosity, and genetic disturbance
due to incomplete coadaptation among genes (Møller and
Swaddle, 1997; Polak, 2003). Variation in developmental
instability should often reflect heritable differences, leading
to selection for mate preferences based on traits that honestly
advertise developmental instability (e.g., scents). The herita-
bility of developmental instability is unknown, despite the
many studies that have been performed, due to low power
(Fuller and Houle, 2003; see also Møller and Thornhill,
1997a,b; Van Dongen, 2000). Based on these studies, Gang-
estad and Thornhill (2003) estimated that the heritability of
developmental instability is, on average, 0.2–0.3.
In humans, FA may be involved in viability-based good-
genes sexual selection. In both sexes, low FA appears to be
associated with increased genetic, physical, and mental health,
including cognitive skill and IQ (Furlow et al., 1997; Thornhill
and Møller, 1997; Yeo et al., 2000). Compared to asymmetric
men, symmetric men seem to be more muscular, vigorous,
and socially dominant (Gangestad and Thornhill, 1997b),
have lower basal metabolic rate (Manning et al., 1997), and
may be larger in body size (Manning, 1995; Gangestad and
Thornhill, 1997b) than asymmetric men. Low FA in men
predicts components of mating success such as a relatively
high number of sexual partners, quicker sexual access to a new
romantic partner (Baker, 1997; Gangestad and Simpson,
2000; Gangestad and Thornhill, 1997b; Gangestad et al., 2001;
Thornhill and Gangestad, 1994), facial attractiveness (Baker,
1997; Gangestad et al., 1994; Thornhill and Gangestad, 1994;
but see also Gangestad and Thornhill, 1997a; Simpson et al.,
1999; Thornhill and Gangestad, 1999b), and number of
extrapair copulation (EPC) partners and number of times
669
chosen as an EPC partner (Gangestad and Thornhill, 1997a).
Moreover, men’s symmetry predicts a relatively high frequency
of their sexual partners’ copulatory orgasms (Thornhill et al.,
1995). Female copulatory orgasm may be a mechanism of
cryptic female choice by selective ejaculate retention in con-
texts in which women mate with multiple partners (see Baker
and Bellis, 1995; Thornhill et al., 1995).
The effect of symmetry on sexual attractiveness appears to
be stronger in men than in women, and it is only in men
that symmetry predicts the components of mating success
mentioned above (Gangestad and Thornhill, 1997a). This
difference is not surprising, as sexual selection has been
stronger in males than females in human evolutionary history
(Buss, 1994; Geary, 1998; Symons, 1979).
Several lines of evidence indicate that olfactory cues or
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pheromones may play a major role in the human sexual
selection system. First, though adults of both sexes report that
body scent of others significantly affects their sexual interest,
women report a stronger effect than men (Franzoi and
Herzog, 1987; Herz and Cahill, 1997; Regan and Berscheid,
1995). Second, evidence suggests that the importance of male
scent in women’s sexual interest and arousal varies across the
menstrual cycle. Women’s olfactory sensitivity to androstenol
and related chemicals appears to be enhanced before
ovulation, near the peak of fertility in the menstrual cycle
(Doty, 1981; Vierling and Rock, 1967; but see Amoore et al.,
1975; see also Pause et al., 1996). Androstenol, a chemical
precursor of androstenone, is an important contributor to
body odor, and its production is highly sexually dimorphic;
men excrete three times more androstenol in urine than
do women (Brooksbank, 1962; Brooksbank and Haslewood,
1961).
Women’s sexual desire for men other than their primary
partner and rate of EPCs also change across the menstrual
cycle, peaking during the midfollicular to ovulatory phases
(e.g., Baker and Bellis, 1995; Gangestad et al., 2002). When
coupled with findings on cycle-related scent preferences,
these shifts suggest a third connection between sex pher-
omones and human sexual selection. Specifically, the fact that
EPCs and associated desire for nonpartner men and positive
evaluation of sexually dimorphic substances in human sweat
peak near maximal menstrual-cycle fertility suggests that
selection has led to a preference in women for their
offspring’s sire and that the preference may include an
olfactory component.
Based on this notion, Gangestad and Thornhill (1998b)
proposed that olfactory stimuli pertaining to men’s pheno-
typic and genetic quality, measured by degree of body FA,
positively affects men’s scent attractiveness to women,
particularly during the fertile phase of the cycle when
expressed preference for offspring’s sire is critical. Three
published studies now support this hypothesis (Gangestad
and Thornhill, 1998b; Rikowski and Grammer, 1999; Thorn-
hill and Gangestad, 1999b). Specifically, all studies show that
the scent of symmetric men is attractive to women who are
cycling normally (i.e., not using hormone-based contra-
ceptives) and are in the fertile phases of their menstrual
cycles. Women using hormonal contraceptives and normally
ovulating women in infertile phases of their cycles appear to
show no preference for the body scent of either symmetrical
or asymmetrical men. This research did not find that men rate
the scent of symmetrical women more attractive than the
scent of asymmetric women. If women’s mid-cycle scent
preference for low FA is caused by a preference for MHC
dissimilarity, then men who, on average, are dissimilar to
many others (for whatever reason) should have low FA.
The research on the scent of men’s symmetry also gave
results suggesting that facial attractiveness (as judged from
670
photos) correlates positively with body scent attractiveness to
the opposite sex in both sexes and that ovulating women’s
preference for the scent associated with men’s facial at-
tractiveness is maximal when their fertility is highest across
the menstrual cycle (Thornhill and Gangestad, 1999b; also see
Rikowski and Grammer, 1999). One theory of human physical
attractiveness is that it reflects, in part, genetic differences in
viability and, from the standpoint of sexual selection, is
preferred partly for this reason (Gangestad, 1993; Thornhill
and Gangestad, 1993). Facial attractiveness, in part, reflects
judging facial hormone markers, which appear to be estrogen
facilitated in women and androgen facilitated in men
(Thornhill and Gangestad, 1999a). The male faces that
women in the fertile phase of their cycle most prefer are
more masculine than the faces they most prefer when in
infertile phases ( Johnston et al., 2001; Penton-Voak and
Perrett, 2001; Penton-Voak et al., 1999). These results raise
the possibility that scent attractiveness may be related to the
chemistry of sex hormones.
Overall, evidence indicates that pheromones are important
in the human sexual selection system. Pheromones appear to
be associated with MHC, men’s FA, sexually differentiated
odor substances, and traits of facial attractiveness. The specific
chemicals that signal MHC, FA, or hormone status may or may
not be shared. (For instance, the scent of low FA may or may
not involve the chemistry of sex hormones; scents associated
with rare or otherwise dissimilar MHC genotypes may or may
not be those associated with the scent of low FA; etc.) Whether
involving the same chemistry or not, the pheromone systems
may or may not be interrelated in functional terms (e.g., they
may or may not all be associated with parasite-mediated
sexually selected signals). To further examine their roles,
including the various hypotheses for MHC-based mate choice,
and to explore their interrelationships, if any, we conducted
a study of men’s and women’s attraction to the body scents of
members of the opposite sex. The MHC of all participants was
genotyped at the A, B, and DRb loci (as in Wedekind et al.,
1995; Wedekind and Füri, 1997). In addition, we measured
the body symmetry of all participants and had facial photo-
graphs of them rated for attractiveness. We recruited for the
study women who did not use contraceptive hormones. The
hypotheses for the MHC-dissimilarity preference all predict
that the preference should be seen at fertile cycle times.
Singh and Bronstad (2001) reported that men prefer the
scent of women who are in the fertile phase of their cycle,
suggesting yet another pheromone-based system of prefer-
ences in humans. We examined Singh and Bronstad’s finding
in the current study.
MATERIALS AND METHODS
With the exception of obtaining a blood sample for MHC
genetic analysis from each research participant and paying
each participant $20, methods were identical to those in the
study of the scent of symmetry by Thornhill and Gangestad
(1999b). Research participants were 97 men and 100 women.
Ages ranged from 18 to 54 for men (mean 6 SD ¼ 23.1 6 6.1)
and 17 to 44 for women (21.2 6 5.5). Self-reported ethnicities
of men were 62% Caucasian, 29% Hispanic, 2% African
American, 5% Asian, 1% Native American, 1% other; of
women, 48% Caucasian, 37% Hispanic, 2% African American,
1% Asian, 6% Native American, 5% other. Most participants
received experimental course credit in an introductory
psychology course in return for their participation in the
research (see Gangestad and Thornhill, 1998b). Some
received grade points in a biology course. Recruitment
postings specifically asked for women who did not use
hormone-based contraception (i.e., birth control pills, Depo-
Behavioral Ecology Vol. 14 No. 5
Provera, or Norplant). We asked women whether they used
a contraceptive of this sort and did not include the responses
of those who did.
Wedekind and colleagues (Wedekind and Füri, 1997;
Wedekind et al., 1995) found a different pattern of MHC
scent preferences for women using contraceptive pills. These
women prefer the scent of individuals with similar MHC
genotypes. The pill is thought to generate a physiological
state like that in pregnancy. Pill-users preference for MHC-
similar scents is not a mate preference, but instead may
be a preference for the smell of genetic relatives who may
assist nepotistically.
The mechanisms of infertility suppression caused by the
three types of hormone-based contraception used by some
women in our study apparently differ (e.g., prevention of
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ovulation or implantation), making it difficult to predict
how women using the various hormone-based contraceptives
should behave in scent-based mate choice. Furthermore,
sample sizes of each of the three hormone-based contracep-
tion users are too small for any meaningful estimates of
effects, if any.
Measurement of FA
Participants reported in unisex groups of up to four for an
initial session. After reading and signing an informed consent
form, each participant was given a brief questionnaire on
demographic and other information (e.g., age, height,
weight, sexual orientation, socioeconomic status of family of
origin, lifetime number of sexual partners). Participants were
scheduled for a later date, at which time they provided a blood
sample (see below). For each participant, the right and left
sides of the following 10 characters were measured using
a digital caliper, sensitive to 0.01 mm: ear length, ear width,
elbow width, wrist width, ankle width, foot breadth, and
lengths of all fingers excluding the thumb. In previous
samples (n . 700), these characters have been shown to
exhibit very little directional asymmetry and slight leptokur-
tosis, as expected of FA (Furlow et al., 1997; Gangestad and
Thornhill, 1999). To assess and increase reliability, we
measured each character twice. In addition, a facial photo-
graph was taken with a 35-mm camera (50 mm lens), placed
approximately 2.5 ft. from the participant’s face (using 400
ASA color film).
After measurements were taken and the questionnaire was
completed, each participant was given a clean, unworn, white,
cotton Hanes-brand t-shirt and provided with explicit wearing
instructions. Each was told that he/she should wear the t-shirt
2 particular nights (identical for each sex) while sleeping.
Each was also instructed to wash his/her bed sheets with
unscented laundry detergent (provided by us) before those
two nights and, during the 2-day period, refrain from (1)
using scented soaps, deodorant, or fragrance such as
perfume, cologne, or aftershave, and instead use only
unscented soap (which we provided); (2) eating garlic, onion,
green chile, pepperoni, pungent spices, herbs, strong cheeses,
cabbage, celery, asparagus, yogurt, and lamb; (3) drinking
alcohol or using recreational drugs; (4) smoking tobacco; (5)
engaging in sex with another person; or (6) sleeping with
another person. Each participant was further instructed to
place the t-shirt in a plastic bag (provided and identified with
an arbitrary code number) during the day, when not worn,
and return the shirt, in the bag, the morning following the
second night at 0900 h. Almost all of male and female
participants returned their shirts on time, allowing their use
in the scent rating phase of the study (see below). When
participants dropped off their shirts, each filled out a brief
questionnaire about guidelines, if any, they had violated
Thornhill et al.
Human scent attractiveness
during the 2-day period when shirts were worn during sleep.
They were told that they would lose no experimental course
credit or grade points for violating any of our instructions,
and that it was important that they be honest. The
questionnaire also asked whether the participant had been
ill, how often he or she had bathed, and whether scented soap
or shampoo were used during the two-day period. Because
we had told participants that, should they happen to use
deodorant during the day, they should shower before putting
on the shirt, we asked whether they had showered before
wearing the shirt.
Scent attractiveness ratings
At 1000 h of the morning that participants of one sex
returned shirts, the opposite-sex participants began reporting
in groups of up to five. Following informed consent, each
woman or man was placed in a separate room for rating the t-
shirts. Shirts had been separated into groups of approximately
10 and each group placed in a box. In addition to the shirts
worn by men and women, one unworn shirt was included in
the sample. Boxes were circulated through the sample of
raters present during a session. Though no attempt was made
to fully randomize the order in which raters smelled shirts, it
is likely that no two raters smelled them in precisely the same
order. For each shirt, raters were asked to open the plastic bag
and, without touching the shirt, smell it and rate the scent on
three dimensions: (1) pleasantness, on a scale of 1 ¼ very un-
pleasant to 10 ¼ very pleasant; (2) sexiness, on a scale of 1 ¼
very unsexy to 10 ¼ very sexy; and (3) intensity, where 1 ¼ not
at all intense to 10 ¼ very intense. They were instructed to roll
the top of the bag shut before putting it back in its box and
moving onto the next shirt. All researchers presenting shirts
to participants for smelling were unaware of the symmetry
scores of the participants who had worn them and of the MHC
genotypes of t-shirt raters and wearers.
Women raters were also given a brief questionnaire to fill
out, which assessed (1) whether the woman currently used
a contraceptive pill or other hormone-based contraceptive;
(2) the first day of the woman’s last menstrual period (women
were provided a calendar to assist with this task); and (3) the
typical length (in days) of the woman’s menstrual cycle. These
data allowed our calculation of the women’s probability of
conception during shirt wearing and rating (see below).
In total, rating sessions lasted about 1 h and were con-
ducted from 1000 until 1600 h the day of and from 0800 to
1500 h the day after the collection of the t-shirts.
Despite our instructions, the smell of fragrance (from
perfume, soap or lotion) or smoke was evident on some shirts.
Scent raters were asked to indicate if they smelled a non-
human odor on any of the shirts. Guided by these comments,
four researchers systematically smelled shirts and confirmed
ones that had such odors. Of women’s shirts, 14 had smell
of fragrance and 4 had smell of smoke. Of men’s shirts, 7
smelled of fragrance and 3 smelled of smoke. In addition, we
asked men and women whether they had broken any rules. An
additional 3 men said that they wore fragrance without
showering, 4 claimed to smoke, and 3 said that they slept with
someone; corresponding numbers for women were 4, 8, and
2. Finally, we asked whether participants had been sick over
the preceding 2 days. An additional 9 men and 8 women
reported sickness. The scent of men who had been sick
tended to be less attractive than other men’s scent (r ¼ .16,
p , .10); sick women did not smell less attractive (r ¼ .12, ns).
As a conservative measure, all these participants’ shirts were
eliminated from analysis. A total of 56 men’s shirts and 48
women’s shirts were used for analysis. (Unlike in a previous
study [Thornhill and Gangestad, 1999b], number of showers
671
taken did not covary with scent attractiveness, and, hence, no
adjustment was made for number of showers.)
Of the 89 women who reported to smell shirts, 21 used the
pill or another hormone-based contraceptive (Depoprovera,
Norplant), 1 was postmenopausal, and 1 did not appropriately
fill in the rating sheet. Also, one woman reported an
exclusively homosexual orientation; because this study exam-
ined attractiveness of scent in a heterosexual situation, we
excluded her from analyses. Of the 77 men who reported
to smell shirts, none reported an exclusively homosexual
orientation. In total, our primary analyses of shirt raters in-
cluded 65 women who did not use hormone-based contra-
ception and 77 men.
Facial attractiveness ratings
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We recruited 14 women and 15 men unfamiliar with the
research to rate participants’ facial attractiveness based on
facial photographs. Ratings were made on a 1 (least attractive)
to 10 (most attractive) scale. Raters were instructed not to rate
pictured individuals whom they recognized. All opposite-sex
ratings were averaged to yield an index of facial attractiveness.
Internal consistency of these indices was high: for male
participants, a ¼ .90; for female participants, a ¼ .86. (We
used opposite-sex ratings only, though mean ratings made
by the two sexes were highly correlated: for male participants,
r ¼ .88; for female participants, r ¼ .88; both p , .00001.)
HLA typing
Approximately 10 ml of whole blood from each subject was
collected by a phlebotomist into Vacutainer tubes containing
EDTA to prevent clotting. Genomic DNA was prepared for
typing by the BioTest SSP System (BioTest Diagnostics
Corporation, Denvile, NJ) following manufacturer’s recom-
mended protocols. DNA was typed by polymerase chain
reaction (PCR) for the HLA-A, B, and DRb loci following the
manufacturer’s recommended protocols. Briefly, this tech-
nique uses allele-specific primers to amplify PCR products. We
determined the presence or absence of a PCR product in each
reaction by resolving the products on 1.5% agarose.
Data treatment: symmetry
Repeatabilities (rIC) for the 10 measures of signed asymme-
tries of individual traits ranged from .79 to .93 for men (all p ,
.00001, mean rIC ¼ .86) and for women from .76 to .93 (all p ,
.00001; mean rIC ¼ .84). For unsigned asymmetries, rIC for
men ranged from .63 to .87 (all p , .00001; mean rIC ¼ .73)
and for women from .60 to .87 (all p , .00001; mean rIC ¼ .74).
Previous analysis on a large sample (n . 700) demonstrated
that the traits studied exhibit at most small directional
asymmetry (see Furlow et al., 1997). As was true in that
sample, only foot width in this study showed significant
but small directional asymmetry (with Bonferroni correction
for number of traits; t192 ¼ 4.22, p , .001; left . right; the
mean  0 ¼ .3 SDs). No signed asymmetry exhibited sig-
nificant platykurtosis, indicative of antisymmetry. Mean g2
was 0.78 across the traits, and hence distributions were
mildly leptokurtic, as expected of FA (see Gangestad and
Thornhill, 1999).
To guard against the effects of large asymmetries due to
injury, FA of traits that participants reported as injured by
break or sprain were excluded in these analyses if they were
greater than the mean (4.6% for men, 1.1% for women). For
measurement purposes, the mean FA for the trait in the whole
sample of participants was substituted in these instances (see
Thornhill and Gangestad, 1994).
672
We calculated an aggregated FA score in two different ways.
First, each trait’s absolute asymmetry was divided by the mean
trait size ([right þ left]/2) for that participant, and the FA of
all 10 characters was summed to yield an overall index
(relative FA). Second, each trait’s absolute asymmetry was
standardized (divided) by the sample mean of trait size and
summed to yield an overall index (absolute FA). These two
measures correlated .97 with each other and yielded nearly
identical results. Thus, we report results for just one measure
(the first) below. The intraclass correlation across the
two measurements for the summed index was .82 for men
(F96,97 ¼ 10.10, p , .000001) and .84 for women (F99,100
¼ 11.13, p , .000001). The mean composite FA was .174 (SD
¼ .052), close to the mean observed in previous studies
(Gangestad and Thornhill, 1999).
Data treatment: scent attractiveness
For women, we estimated fertility (probability of conception
following sex) on the basis of their day of the cycle and
conception values reported in the medical literature (Baker
and Bellis, 1995; Jöchle, 1973). We did so in two ways, one
based on a forward method, the other on a backward method
(see Baker and Bellis, 1995). For the forward method, we
simply took the day of the cycle that women were at on the
day of smelling based on their reported first day of last
menstruation and used the actuarial table to estimate
probability of conception. For the backward method, we took
into account women’s reported cycle length (mean ¼ 27.9
days, SD ¼ 4.0; average of two reports, which correlated .82,
p , .0001). Women who have longer cycles, on average, ovulate
later in the cycle than women who have shorter cycles
(Baker and Bellis, 1995). We assumed that the typical day of
ovulation was about 15 days before the end of their typical
cycle (e.g., day 14 in a 29-day cycle) and that the average
day that actuarial tables are based on is day 14. Women’s
probability of conception was then based on how far they
had come toward or after their assumed day of ovulation
and the actuarial tabled values for women in general. The
two methods yielded values that correlated .62 (p , .0001),
and results based on each were highly similar. As each
method may have some validity that the other lacks, we
averaged the two sets of values for our main analyses. (Full
results are available from the authors.) The minimum value
was .01, the maximum .39 (approximately day 12 of the
cycle). Fertility steeply rises from near-zero to near .2 shortly
after the average end of menses (days 5–6) and sharply falls
from ..2 to ,.1 immediately after mean ovulation (day 14).
Undoubtedly, our method of estimating conception risk is
likely to be in error for some individual women (though,
across all women, it should correlate highly with actual
risk). As it is unlikely that error introduced by our method
spuriously generates significant relationships, the associa-
tions we report probably underestimate rather than over-
estimate true relationships with conception risk.
The mean correlation between individual participants’
‘‘pleasantness’’ and ‘‘sexiness’’ ratings was .78 for women
raters and .82 for men. Hence, these ratings were averaged for
each sex into a total attractiveness index for reported analyses.
Analyses on specific ratings yielded highly similar results.
Data treatment: MHC genetics
MHC similarity for individual male–female pairs was com-
puted as the total number of alleles shared across the three
loci. Hence, if both individuals were A1, A3 at the A locus,
similarity for that locus was scored 2. If one individual was
homozygous for A1 and the other was A1, A3, similarity was
Behavioral Ecology Vol. 14 No. 5
scored 1. If both individuals were homozygous for A1,
similarity was scored 2. Similarity scores could thus range
from 0 to 6. Actual similarity for pairs averaged 1.25 alleles
(SD ¼ 0.37). MHC heterozygosity was the number of loci at
which the participant was heterozygous. Mean heterozygosity
was 2.69 (SD ¼ 0.54).
Because our multiethnic sample may have unique charac-
teristics, MHC allele frequencies were calculated within the
sample. Total number of allele observations within the sample
was 352, 348, and 348 for the A, B, and DRb loci, at which
we detected 20, 28, and 14 different alleles, respectively. Rela-
tive frequencies of all alleles are given in Figure 1. We com-
puted the commonness of a participant’s alleles as the
proportion of alleles within the sample of the type possessed
by the participant, averaged across the participant’s six alleles.
Commonness scores averaged 0.113 (SD ¼ 0.032, range ¼
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0.04–0.21).
RESULTS
For all scent effects that have been found in prior research on
humans (preference for the scent of MHC dissimilarity,
women’s preference for the scent of symmetrical men when
fertile, preference for the scents of facially attractive individ-
uals, men’s preference for the scent of fertile women), we
used directed tests (Rice and Gaines, 1994), which use a p
value of .04 for a predicted relationship and .01 for
a relationship opposite of prediction (rather than .025 for
each, as with a two-tailed test). All directed tests are labeled
as such. In all other instances, we used two-tailed tests.
Although unsigned (i.e., absolute) FA tends to be non-
normally distributed (Swaddle et al., 1994), Monte Carlo
analyses reveal that significance tests on parametric correla-
tions involving FA are robust (Gangestad and Thornhill,
1998b), and hence we performed standard parametric anal-
yses on this variable.
Descriptive statistics
On average, men’s scents were rated 4.54 (SD ¼ 0.95) on the
1–10 attractiveness scale. Women’s shirts received a mean
rating of 4.71 (SD ¼ 0.63). There was no significant sex
difference in mean scent attractiveness (t102 ¼ 1.08). Men’s
shirts tended to receive more variable ratings than did
women’s shirts, though this difference was only marginally
significant (F1,102 ¼ 2.94, p ¼ .089; Levene’s test for equality of
variances). On average, men rated the unworn t-shirt’s scent
attractiveness 3.82 and women rated it 4.02. On average,
women’s and men’s scents were rated by the other sex as
more attractive than the blank shirt’s scent (t76 ¼ 4.97 and
t64 ¼ 3.38, respectively, p , .002).
Preferences for MHC dissimilarity
Analyses that treat the t-shirt wearer as the unit of analysis
(and examine whether raters who possess dissimilar MHC
genotypes rate their scents more favorably) control for factors
that contribute to overall differences in scent attractiveness
and, hence, should offer the greatest power to detect
preferences for MHC dissimilarity (Wedekind and Füri,
1997). Using the procedures of Wedekind and Füri (1997),
we computed for each t-shirt wearer a correlation between
individuals’ ratings of scent attractiveness and the number of
MHC alleles shared between the t-shirt wearer and the rater.
We then asked whether these correlations differed signifi-
cantly from zero in the predicted negative direction.
We found no evidence that men’s scents were preferred
by women with dissimilar MHC genotypes (mean r ¼ .025,
Thornhill et al.
Human scent attractiveness
Figure 1
Relative frequencies of MHC alleles at A, B, and DRb loci.
t54 ¼ 1.39, directed). In contrast, we did find women’s scents to
be preferred by men with dissimilar MHC genotypes (mean r ¼
.033, t47 ¼ 1.74, directed p ¼ .040). The mean correlations
significantly differed from one another (t101 ¼ 2.30, p ¼ .024),
revealing a sex difference in the preference for MHC
dissimilarity. Specifically, the attractiveness of women’s scents
to men appears to be positively influenced by MHC
dissimilarity to a degree greater than the attractiveness of
men’s scents to women.
Analyses that treated the scent rater as the unit of analysis
(and examined whether raters prefer the scents of those with
dissimilar MHC genotypes) were also conducted. We com-
puted raters’ preference for dissimilar MHC as the slope of
their ratings regressed on MHC dissimilarity (b). For neither
men nor women raters did we find evidence of preference for
MHC dissimilarity: For men, mean b ¼ .007, t69 ¼ .42, directed
ns; for women, mean b ¼ .051, t61 ¼ 1.41, directed ns. The
mean preferences for the two sexes did not differ (t130 ¼
1.17). Again, these analyses are less powerful than those
treating the t-shirt wearer as the unit of analysis, which may
account for the difference in results.
Despite no evidence for an overall preference in women for
the scent of MHC-dissimilar men, women’s preference for
MHC dissimilarity could be moderated by their fertility status
across the menstrual cycle. However, we found no evidence of
a role for fertility status. Women’s probability of conception
across the cycle had a near-zero correlation with their
preference for MHC dissimilarity (r ¼ .029, directed).
Possibly, preference for dissimilarity is not a linear function.
Perhaps, for instance, a moderate degree of dissimilarity is
preferred, with high levels of similarity and dissimilarity
disfavored (see Penn, 2002). If that is the case, then targets’
mean level of MHC sharing with others should predict, for
individual targets, the correlation between the target’s MHC
sharing with a rater and the rater’s attraction to the target’s
scent: those targets who, on average, share relatively many
673
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MHC alleles with others (i.e., because they have common
alleles) should be particularly preferred by those who are
dissimilar, whereas targets who, on average, share few MHC
alleles with others (i.e., because they have rare alleles) should
be more preferred by those who are relatively similar (e.g.,
share even a single allele). This hypothesis was not supported.
For the 48 female targets, the association ran in the direction
anticipated if there were a preference for the scent of those
with moderately similar MHC genotypes, but fell short of
significance (r ¼ .19). For the 55 male targets, the associa-
tion between their mean MHC sharing with others and the
correlation between raters’ attraction to their scent and MHC
sharing with the target ran in the opposite direction (r ¼.38,
p , .01). (Hence, the scent of men who had rare MHC alleles
and therefore shared relatively few alleles with men were
more likely to be preferred by women with dissimilar MHC
genotypes.) These correlations significantly differ from one
another (z ¼ 2.91, p , .01).
Preferences for symmetry
As in previous research (Gangestad and Thornhill, 1998b;
Thornhill and Gangestad, 1999b), we calculated a preference
for the scent of symmetry for each woman, which is the slope
of the woman’s scent attractiveness ratings regressed on men’s
symmetry (with positive values reflecting preference for
symmetry and negative values preference for asymmetry).
We correlated these preferences with women’s probability of
conception. Consistent with previous studies, women’s pref-
erence for symmetry was predicted by their fertility status (r ¼
.269, directed p ¼ .019). Regression analyses revealed that, at
zero probability of conception, women had a significant
preference for symmetry (t63 ¼ 2.45, p , .017), a pattern
unique to this study. Moreover, this preference for symmetry
increased as a function of their conception risk (see Figure 2).
Mean scent-attractiveness ratings made by women (n ¼ 22)
674
Figure 2
Preference of normally ovulating (not using hormone-based contra-
ception) women for the scent of symmetry as a function of their
probability of conception, based on values reported in the medical
literature (Baker and Bellis, 1995; Jöchle, 1973); r ¼ .269, p ¼ .019.
who had conception risks of at least 0.15 (day 6–day 14)
correlated (.29; directed p ¼ .02) with men’s FA, whereas
mean ratings made by all other women (n ¼ 27) were more
loosely correlated (.11; ns) with men’s FA; these correlations
significantly differed from one another (t53 ¼ 2.57, p ¼ .008).
Women’s conception risk did not significantly correlate with
the mean rating they gave all scents (r ¼ .04, ns) or the
rating they gave the unworn shirt’s scent (r ¼ .06, ns). As also
found by Thornhill and Gangestad (1999b), women’s mean
scent attractiveness to men did not correlate with women’s FA
(r ¼ .063, ns).
Preferences for MHC heterozygosity
We examined preferences for MHC heterozygosity by corre-
lating the number of MHC loci at which individuals were
heterozygotes with their mean scent attractiveness to the
opposite sex. Male heterozygosity was positively correlated
with scent attractiveness (r ¼ .275, p ¼ .049). Follow-up
analyses showed that this effect was driven by heterozygosity at
the B locus (r ¼ .329, p ¼ .017); no effect was observed for
either the A or DRb locus (r ¼ .025 and .161, respectively,
ns). As these correlations do not significantly differ from one
another, however, these locus-specific differences may not be
robust and must be interpreted cautiously. Female heterozy-
gosity did not predict scent attractiveness (r ¼ .004, ns). Sex
did not interact with heterozygosity to predict scent attrac-
tiveness (t93 ¼ 1.56, p ¼ .12).
We examined whether women’s preferences for heterozy-
gosity change across the menstrual cycle. These preferences
were calculated as the slope of women’s ratings regressed on
men’s MHC heterozygosity. They correlated with women’s
probability of conception at a level just short of statistical
significance(r ¼ .239, t63 ¼ 1.96, p ¼. 055), such that women
outside of the fertile phase tended to have the strongest scent
preferences for heterozygosity. The correlations of women’s
preference for symmetry and preference for heterozygosity
with conception risk differed significantly from one another
(t62 ¼ 2.87, p ¼ .006), indicating that these female preferences
at least partly invoke different systems.
Preferences for rare MHC alleles
We examined preferences for rare MHC alleles by correlating
the mean frequency of MHC alleles within this sample across
Behavioral Ecology Vol. 14 No. 5
Table 1
Correlations between FA, facial attractiveness, and MHC variables
Men Women
Facial Facial
attractiveness FA attractiveness FA
Mean MHC dissimilarity
to others .084 .045 .078 .066
MHC heterozygosity .066 .096 .137 .161
Mean commonness of
MHC alleles .093 .127 .155 .089
All correlations ns. Correlation between FA (fluctuating asymmetry)
and facial attractiveness: .086 for men, .029 for women, ns.
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the six alleles an individual possesses at the three loci with
mean scent attractiveness. For women, commonness of alleles
significantly predicted the attractiveness of their scents, such
that those with more common alleles tended to have more
attractive scents (r ¼ .309, p ¼ .032). Men’s scent attractive-
ness was not associated with the commonness of their alleles
(r ¼ .025, ns). Sex did not significantly moderate the
relationship between commonness of alleles and scent
attractiveness (t96 ¼ .980). Women’s preferences for rarity of
MHC alleles (calculated as the slope of their ratings regressed
on men’s MHC allelic rarity) did not significantly covary with
their fertility status (r ¼ .132).
Preference for the scent of facial attractiveness
As found in previous studies (Rikowski and Grammer, 1999;
Thornhill and Gangestad, 1999b), women’s facial attractiveness
predicted their scent attractiveness (r ¼ .268, directed p ¼
.041). Unlike in the previous studies, men’s facial attractiveness
did not predict their scent attractiveness (r ¼ .053, directed
ns). Nonetheless, sex did not significantly moderate the
relationship between facial and scent attractiveness (t100 ¼
1.30).
Previously, Thornhill and Gangestad (1999b) found that
women’s probability of conception predicted their preference
for the scent of facially attractive men. In this sample, though
the correlation was in the same direction, no significant
association emerged (r ¼ .096, directed). In this sample,
FA did not predict men’s or women’s facial attractiveness
(r ¼ .086 and .029, respectively, ns).
Male preferences for fertile women
Women’s estimated probability of conception at the time of
wearing the t-shirt was correlated with their mean scent
attractiveness. As found by Singh and Bronstad (2001), men
were more attracted to the scents of women of high fertility
status than those of low fertility status (r ¼ .334, directed
p ¼ .021).
Associations of FA and facial attractiveness with MHC
dissimilarity, heterozygosity, and commonness of alleles
Neither FA nor facial attractiveness was significantly predicted
by mean MHC dissimilarity to others, MHC heterozygosity, or
commonness of MHC alleles within either sex (see Table 1).
These findings bolster the conclusion that, to the extent that
the scent of MHC dissimilar individuals is favored, the
phenomenon is unrelated to women’s preference for the
scent of symmetrical men when fertile. They also add further
evidence that women’s scent preference for men who are
heterozygous at MHC sites is distinct from their scent
preference for symmetrical men.
Thornhill et al.
Human scent attractiveness 675

Additional analyses on the whole sample. Our finding (based on the whole
sample) that ethnicity has no effect on scent attractiveness in
For exploratory purposes, we correlated men’s mean scent
either sex suggests that our results on MHC scent effects are
attractiveness rating with their age, weight, and self-reported
meaningful. However, our ethnic categorization was self-
socioeconomic status of family of origin (on a 5-point scale,
reported using broad categories.
where 5 ¼ upper class, 3 ¼ middle class, 1 ¼ lower class).
These correlations were not significant (r ¼ .04, .21, and .08,
respectively). For women, mean scent attractiveness correlat- The scent of symmetry
ed at a marginally significant level with age (r ¼ .28, p ¼ .058
Compared to the body scent of relatively asymmetric men,
and socioeconomic status, r ¼ .26, p ¼ .077, but not with
relatively symmetrical men’s scent is most attractive to
weight, r ¼ .10, ns). Analyses comparing scent attractiveness
normally ovulating women (women not using hormonal
of men and women across ethnicities revealed no significant
contraception) during their period of high fertility in the
differences (F5,50 ¼ .44 and F4,47 ¼.38).
menstrual cycle. We have found little evidence that women
We conducted additional exploratory analyses. We corre-
show scent preference related to male body symmetry during
lated preference for the scent of symmetry with the judge’s
cycle times of low fertility. In this study only, and not in the
own scent attractiveness, age, FA, physical attractiveness, and

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number of self-reported sex partners. Younger women par-
ticularly preferred the scent of symmetrical men (r ¼ .34, p ¼
.005), even with women’s conception risk controlled (r ¼ .30,
p ¼ .015). In contrast, older men particularly preferred the
scent of symmetrical women (r ¼ .24, p ¼ .045). These
correlations significantly differ(z ¼ 3.42, p , .001). Men
whose scent was rated as less attractive also preferred the scent
of symmetrical women (r ¼ .38, p ¼ .009; n ¼ 48 for this
analysis). Women’s scent attractiveness did not predict their
preference for the scent of symmetry (r ¼ .14, ns). Again,
the correlations significantly differed between the sexes (z ¼
2.18, p , .03). No other correlations were significant. We
correlated women’s preference for MHC dissimilarity, MHC
heterozygosity, and MHC allele frequency with the same
variables. Only a single correlation was significant (men’s age
negatively predicted their preference for heterozygosity), one
that could easily be due to chance.
Older and more facially attractive men particularly pre-
ferred the scent of women near ovulation (r ¼ .23 and .25, p ,
.05). Men’s preferences tended to covary with one another.
Men’s preference for the scent of symmetrical women was
negatively associated with their preference for MHC hetero-
zygotic women (r ¼ .32, p ¼ .004). Their preference for
women near peak fertility also negatively predicted their
preference for heterozygotic women as well as their prefer-
ence for women with rare MHC alleles (r ¼ .24 and .26,
p , .04). Finally, men’s preference for the scent of MHC-
dissimilar women was negatively associated with their prefer-
ence for facially attractive women (r ¼ .36, p ¼ .003).
(Preference for MHC dissimilarity also predicted preference
for rare MHC alleles [r ¼ .32, p ¼ .006], an association that is
not surprising, as women with rare alleles are relatively
dissimilar to men at MHC.) No female preferences signifi-
cantly correlated with one another.
DISCUSSION
This study used t-shirts worn by each sex for 2 night’s sleep
and then smelled by the opposite sex to examine the
relationships between heterosexual attractiveness of one’s
body odor and one’s body fluctuating asymmetry (FA), facial
attractiveness, MHC dissimilarity, MHC heterozygosity, and
possession of rare MHC alleles. Our results address four
adaptive hypotheses that have been proposed for scent-based,
MHC disassortative mate preferences: outbreeding, produc-
tion of MHC-heterozygous offspring or of offspring with rare
MHC alleles, and increased within-brood MHC diversity.
Additionally, our results address issues concerning the prior
finding that women, when fertile in their menstrual cycle,
particularly prefer the scent of symmetrical men.
MHC allele frequencies may differ among ethnic groups.
Our sample was multiethnic, and we based allele frequencies
studies of Gangestad and Thornhill (1998b) and Thornhill
and Gangestad (1999b), women with zero conception risk
exhibited a significant preference for the scent of symmetry.
That women at high conception risk in their menstrual cycles
prefer the scent of male symmetry has now been found in four
separate studies (also see Gangestad and Thornhill, 1998b;
Rikowski and Grammer, 1999; Thornhill and Gangestad,
1999b). Although not examined in this study, prior studies
have consistently found that women using hormone-based
contraception do not show the preference for the scent of
men’s symmetry. Moreover, the effect of the scent of symmetry
appears to be sex-specific. We found no evidence that men
find the scent of symmetrical women more attractive, a result
that replicates that of Thornhill and Gangestad (1999b).
Apparently, the attractiveness of the symmetry scent to
women does not arise from hygienic differences between men
in relation to their symmetry (e.g., number of times they
showered; see Thornhill and Gangestad, 1999b). Nor does it
appear to arise from not following our research guidelines for
diet, alcohol and drug use, or sleeping behavior over the
period in question (see also Thornhill and Gangestad,
1999b). The symmetry of men was unknown to the women
rating scents and to the researchers involved in collecting the
scent ratings; the only identifying information on the plastic
bag containing each shirt was an arbitrary participant number.
Although women exhibit increased olfactory sensitivity during
the fertile aspect of the menstrual cycle (Doty, 1981; Kohl and
Francoeur, 1995; Vroon, 1997), the odor preference for
symmetry shown by normally ovulating women cannot readily
be explained by an increased general olfactory sensitivity or
response with high fertility. There is no significant relation-
ship between women’s intensity ratings of the shirts and
male symmetry (Gangestad and Thornhill, 1998a; Thornhill
and Gangestad, 1999b). In sum, we know of no explanation
for our results other than that normally ovulating women
use a chemical(s) in men’s sweat or skin as a basis for
discriminating men who have and have not experienced
perturbations that generate FA. Thornhill and Gangestad
(1999b) provided a number of hypotheses about the
chemistry of the scent of men’s symmetry.
Fertile women’s preference for the scent of symmetry may,
in part, account for the pattern of pair-bonded women
tending to choose symmetric men as EPC partners. Given that
symmetric men appear to invest less in their romantic re-
lationships than asymmetric men, these choices are probably
for genetic benefits rather than for increased male investment
(Gangestad and Thornhill, 1997a,b).
Conceivably, the scent of symmetric men is preferred by
women at mid-cycle because of a preference for adequate
sperm. Manning et al. (1998; also Baker, 1997) have shown
a positive correlation between ejaculate size, sperm quality,
and body symmetry in men. This, however, is not necessarily
an alternative to good-genes choice.
676
Preferences for MHC dissimilarity
The results from our study of the scent attractiveness of MHC
dissimilarity repeated, in part, earlier studies. Our study
reveals that men find the scent of MHC dissimilarity attractive,
but we detected no clear MHC-dissimilarity preference in
women. The sex difference in preference for MHC dissimi-
larity was statistically significant. Overall, then, there is positive
evidence of MHC-dissimilarity preference exhibited by men
from both of the t-shirt studies that have examined it
(Wedekind and Füri, 1997; present study). Women have
shown an MHC-dissimilarity preference in two of three t-shirt
studies that tested for it (positive in Wedekind et al., 1995;
Wedekind and Füri, 1997; negative in present study). The
negative assortative pairing in Hutterite couples reported by
Ober et al. (1997) could be the result of an MHC dissimilarity
preference in only one sex or both sexes and hence does not
shine any light on the issue of the consistency of the effect in
each sex. Given that our study had a larger sample of women
wearing shirts and more raters than either study showing
a positive effect for women’s scent and detected an MHC-
dissimilarity effect for men, the absence of an effect for
women may be meaningful. However, the two t-shirt studies
finding an effect for women involved an ethnically homoge-
neous sample that may have reduced individual differences in
odor preferences unrelated to MHC; these two studies also
differed from our study in some other ways.
We did not find any evidence of a relationship between
women’s conception risk across the menstrual cycle and their
preference for the scent of MHC dissimilarity. Thus our results
indicate that women at high risk of conceiving do prefer the
scent of symmetry but not the scent of MHC dissimilarity.
It should be kept in mind, however, that Wedekind and
colleagues found scent preference for MHC dissimilarity in
women at relatively high conception risk, but none for women
who were infertile due to contraceptive-pill use.
Based on our results, we conclude that men’s scent of
symmetry and men’s scent of MHC dissimilarity involve
different pheromonal systems, at least in part. This conclusion
is bolstered by the fact that FA and mean MHC dissimilarity to
others does not covary across individuals (of both sexes).
Either different chemicals activate one receptor adaptation or
multiple receptors are involved, each with chemical specificity.
The receptor responsible for detecting the scent of symmetry
would appear to be sexually dimorphic in function or present
only in females. Furthermore, the sensitivity of this detector
may be affected by menstrual cycle hormones. At least two
different organs appear to mediate scent perception in
humans: the vomeronasal organ (e.g., Wysocki, 1989) and
the main olfactory epithelium (Engen, 1982).
Because women’s attraction to the scent of men’s symmetry
is only seen in normally ovulating women at high conception
risk, it has been hypothesized that this attraction is an
adaptation that functions to obtain for offspring genes that
encode developmental stability and related overall fitness,
particularly through EPC (Gangestad and Thornhill, 1998b;
Thornhill and Gangestad, 1999b, 2003). The lack of a detect-
able association between women’s preference for MHC
dissimilarity and conception risk suggests that the MHC
preference does not involve good-genes mate choice because
the benefit of choosing good genes—placement of a mate’s
genes in offspring at conception—cannot be gained in the
absence of preference during times of high-conception risk.
This interpretation also applies to what some investigators
would label compatible genes (Penn, 2002; Zeh and Zeh,
2001). The interpretation that good-genes (including com-
patible-genes) mate choice is not the basis of women’s MHC-
dissimilarity preference is further supported by our finding
Behavioral Ecology Vol. 14 No. 5
that men have stronger preference for MHC dissimilarity than
do women. If MHC-disassortative mating functions to obtain
good genes for offspring, women are expected to exhibit
a stronger preference than men. These lines of evidence,
then, weaken the three parasite-mediated sexual selection
hypotheses as explanations for MHC preferences.
Nonetheless, a good-genes–choice hypothesis could still
apply if women’s preference for MHC dissimilarity at midcycle
is only manifested under conditions in which the benefits of
good-genes mate choice can be realized (e.g., when diseases
are prevalent). Such conditionality in the preference may
have been selected in the context of EPC due to the
concomitant high potential costs (e.g., divestment of pair-
bond mate). There is evidence for conditionality in the MHC-
odor system of mice. Mice infected with mouse hepatitis virus
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produced more MHC-heterozygous offspring than sham-
infected mice, which may result from the expression of the
MHC-dissimilarity preference only when a virus threatens
offspring (Rülicke et al., 1998).
A stronger scent preference in males for MHC dissimilarity,
as well as the absence of a link between conception risk and
this preference in women, is also inconsistent with the
inbreeding avoidance hypothesis. Females are expected to
have a higher cost of inbreeding than males as a result of
more female than male parental investment.
One possible explanation for why MHC preferences appear
to be stronger in men than women is that they partly function
in men to increase ability to invest discriminatively in their
own offspring. Both sexes may partly use odors of offspring to
detect kinship (Gall and Weisfeld, 2001). Potentially, a male
could most reliably detect by olfaction his own MHC alleles in
offspring if he shares few alleles with his mate.
Preferences for MHC heterozygosity
MHC heterozygosity was not correlated with either facial
attractiveness or with FA in either sex. Heterozygosity is
sometimes positively associated with relatively low FA across
species, and there are data suggesting this association from
some studies of humans (reviewed in Møller and Swaddle,
1997; Thornhill and Møller, 1997).
Women appear to prefer the scent of MHC-heterozygous
men. Furthermore, a trend in the data suggests that women
may prefer the scent of MHC-heterozygous men particularly
when outside of the fertile phase of the cycle. Women’s scent
preference for MHC heterozygosity may be analogous to the
female stickleback’s scent preference for males with high MHC
diversity found by Reusch et al. (2001). We found no evidence
that men have a scent preference for MHC heterozygosity.
If future research confirms a greater female preference for
the scent of MHC-heterozygous men outside of the fertile
phase, two alternative explanations appear plausible. First,
the function of choosing a heterozygous mate could be to
diversify a brood’s MHC, thereby reducing the chances of a
within-family epidemic caused by a pathogen. This preference
would be more important for choosing a long-term mate (i.e.,
one with whom a female would have multiple offspring), and
selection for the preference may have been stronger on
females than on males. The preference may be attenuated
midcycle because other preferences, such as preferences for
intrinsic genetic quality, increase in potency at that time.
Second, infertile women’s preference for heterozygous mates
may reflect adaptation for securing male material benefits for
self and/or offspring. If heterozygosity increases survival or
vigor, it might promote male investment capability. Although
we found no evidence that MHC heterozygosity is associated
with developmental instability, it could be associated with
Thornhill et al.
Human scent attractiveness
disease resistance (see Penn et al., 2002; Penn and Potts,
1999). Given the substantial MHC diversity that exists, MHC
heterozygosity should be only weakly heritable and hence
not be the basis of mate choice for producing heterozygous
offspring. In either case, as the correlation between women’s
conception risk across the cycle and women’s preference for
the scent of symmetry differed significantly from the cor-
relation between conception risk and preference for hetero-
zygosity, the two preference systems may involve distinct
pheromone systems, at least in part.
Preferences for rare alleles
We found no evidence that either sex prefers scents associated
with rare MHC alleles. Indeed, men in our study preferred
scents associated with common MHC alleles. No association
between women’s conception risk and preference for the scent
of rare MHC alleles was detected. A rare-allele preference is
predicted from the hypothesis that MHC-dependent mating
preferences function to generate offspring that have reduced
autoimmune problems (associated with common MHC
alleles) or that cannot be invaded by parasites as a result of
possessing alleles to which parasites are not well adapted.
Gestational drive (Haig, 1997), in which a maternal allele
disfavors offspring during gestation that do not inherit it,
could account for a sex difference in preference for the scent
of common alleles. Gestational drive is delayed meiotic drive
and, like meiotic drive, is advantageous to the alleles involved,
but disadvantageous to the remainder of the maternal
genome. Gestational drive may especially be a property of
rare female alleles because any driving effects of common
alleles are likely to be successfully countered by the evolution
of genes that prevent driving. A mate preference in males for
females who possess common MHC alleles may function to
avoid mates with alleles that show gestational drive and
thereby reduce the likelihood of abortion of offspring.
Females do not face this problem in mate choice.
MHC allele rarity did not covary with symmetry in either
sex. It was previously hypothesized that the scent attractive-
ness of men’s symmetry could arise if symmetric men possess
rare MHC alleles and women prefer rare or dissimilar MHC
alleles (Gangestad and Thornhill, 1998b; Thornhill and
Gangestad, 1999b). This study provides no support for this
hypothesis.
Preferences for scents associated with facial attractiveness
Women’s facial attractiveness, but not men’s, significantly
correlated with body scent attractiveness. Three studies to
date have reported this association for women (also see
Rikowski and Grammer, 1999; Thornhill and Gangestad,
1999b), indicating that women’s facial attractiveness and scent
attractiveness convey overlapping information.
Our study did not replicate the finding from two previous
studies that women with high conception risk prefer the scent
of facially attractive men (Rikowski and Grammer, 1999;
Thornhill and Gangestad, 1999b). The association between
men’s facial attractiveness and their masculinity varies across
populations and samples (for a review, see Thornhill and
Gangestad, 1999a), which may partly account for the instability
of this finding. Possibly, women prefer the scents of more
androgenized men midcycle (due to androgen-derived sub-
stances in sweat; e.g., Grammer, 1993), but in some samples
these men are not the most attractive in terms of scent.
Facial attractiveness was not significantly correlated with
MHC dissimilarity, MHC heterozygosity, or commonness of
MHC alleles in either sex and hence may be independent of
these MHC traits.
677
Men’s preferences for women at high conception risk
We also found that men exhibit significant scent preferences
for women who are at high conception risk in the menstrual
cycle. Using a within-subject design, Singh and Bronstad
(2001) previously found evidence for this preference. Using
a between-subject design similar to the current study, we
previously did not find this preference (Thornhill and
Gangestad, 1999b). The within-subject design is statistically
more powerful (as it controls for individual variation in scent
across women), and we suspect that the variation in this result
is due to the lower power of our between-subject design. The
chemical basis for this effect is unknown. The scent of
chemicals similar to estrogen evoke hypothalamic responses
in men, but not in women (Savic et al., 2001), which may
mediate this effect. Alternatively, the effect could involve
Downloaded from beheco.oxfordjournals.org at Santa Monica College Library on October 4, 2010
variation in copulins present in women’s vaginal secretions.
There is some evidence that men show an olfactory, sexual
response to copulins (Grammer and Jutte, 1997).
We thank P. Andrews, T. Armijo-Prewitt, M. Aronov, C. Fincher, K.
Ganster, K. Schancer, C. Schwenke, S. Singh, N. Terpstra, and J. Vigil
for their assistance in measuring participants, collecting other data,
and data entry. C. Copelin’s extra effort and professional attitude
allowed blood samples to be obtained from almost all our research
participants. The research was supported by a grant from the Sense of
Smell Institute (formerly known as the Olfactory Research Fund). C.
Fincher, D. Penn, C. Wedekind, R. Ydenberg, and two anonymous
reviewers provided useful comments on the manuscript.
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